Berry Go Round #48

This month's Berry Go Round, the botanical blog carnival, is up at Jessica Budke's Moss Plants and More. As a survey of this month's botanical blogging, it's got everything you'd ever want: the curious history of an accidental botanist and his impact on our knowledge of the flora of Wyoming, a discussion on the new USDA plant hardiness maps (aside: I note that I'm still stuck in the anomalous Zone 5b bubble in central Ohio surrounded by Zone 6a), and an amazing blog dedicated to illustrating a botanical word a day. My post from earlier this month about the carnivorous habits of Philcoxia was also featured.

Thanks to Jessica for putting this month's Berry Go Round together. Take some time to check out each of the links presented this month.

Philcoxia: The plant that ate the nematode on subterranean leaves

Could it be? Do we have confirmation of a new genus of carnivorous plants? Possibly. The small genus Philcoxia, which is endemic to Brazil and consists of only three diminutive species, was only just described in 2000. Even in the original description of the plants, authors were noting stalked glands and sticky leaves with later studies observing dead nematodes covering the leaves. These were just hints at the possibility that the plants were deriving some benefit from trapping and killing the wee-beasties and thus might be true carnivorous plants. Definitions vary, but for a plant to be considered carnivorous, it must be demonstrated that the plant has adaptations to (sometimes) lure, trap, and digest prey, absorb the nutrients, and crucially, derive some benefit from it.

Philcoxia minensis - source: Pereira et al., 2012.

But let's back up here. What did we know before this study? Philcoxia grows in nutrient-poor sandy soils, oddly holding its leaves at or just below the ground surface so that the leaves are often covered with sand grains. They have poor root systems, aren't very tall even when in flower, and usually have 5-10 leaves on each plant. When the leaves were examined closely, they were covered in dead nematodes, captured by the sticky secretions among the stalked glands on the upper surface of the leaf.

Sounding familiar yet? To anyone that's acquainted with the other flypaper-type carnivorous plant traps like the sundews (Drosera) and butterworts (Pinguicula), the above description checks all of the boxes for what you'd look for in a carnivorous plant: the need to derive nutrients from sources other than soil, sticky leaves with stalked glands, often ephemeral habits. Most important until this point was the direct observation of nematode prey, published in a 2007 article. The poor nematodes didn't know what hit them; they were mindlessly searching for a brunch of bacteria and they ended up on the menu instead. The 2007 study tested for a common digestive enzyme, proteases, that are often a hallmark of carnivorous plants but detected none, noting, of course, that absence of proteases did not preclude the possibility that Philcoxia was carnivorous after all.

Typical habitat of P. minensis at Serra do Cabral, Minas Gerais, Brazil.
Source: Fritsch et al., 2007

The present study by Pereira et al. (2012), published online ahead of print in PNAS, finally digs deeper and provides us with more experimental evidence. The authors went out into the field, collected plants of P. minensis, and acclimated them to the greenhouse. In what has become standard procedure for determining movement of nutrients from prey to plant, the authors fed 15N-labeled C. elegans nematodes to the plant and left it for 48 hours. The presence of the isotope in the plants cleared of all nematodes after that period of digestion easily indicates that the source of the 15N was the nematode. Compared to controls where no nematodes or nematodes reared without the isotope were fed to the plant, a significant 15% of the isotope originally found in the prey was now found in the leaf biomass after 48 hours. The increase in 15N was associated with an overall increase in nitrogen content of the leaf. My only criticism here is that sample size for all treatments was relatively low at n = 8 and thus the standard error bars are large, though I fully recognize that this is a difficult species to cultivate. I'm also likely spoiled by my time in a microbiology lab where sample size was almost never a problem. As preliminary evidence, this is quite promising! (Out of curiosity, I would have loved to see data on 15N from parts of the plant other than the leaves, since transport of nutrients would be efficient in that 48 hour period.)

While absorption of labeled nutrients from nematode prey is an indication of foliar uptake of nutrients, Pereira et al. conclude that this is also evidence for digestion via the plant's own digestive enzymes. (As an aside, I note that foliar absorption of mineral nutrients is common in plants.) This is a bigger leap from evidence to conclusion and isn't well supported. What we know from Pereira et al. is that the leaves do produce lots of phosphatases, another one of the digestive enzymes that indicates carnivorous activity. It's an easy inferential leap to make from presence of phosphatases and assumed absence of bacterial activity on the leaf's surface in the greenhouse experiment that could otherwise explain the mineralization instead of direct action of the plant. It would be difficult, but ideally Philcoxia should be grown in tissue culture in the absence of bacteria, then be fed the isotope-labeled nematodes for the most convincing data to support the idea of digestion via the plant's enzymes alone.

A group of P. minensis leaves in the sand.
Source: Pereira et al., 2012

The authors also measured neighboring noncarnivorous plants in the field and noted that Philcoxia has a significantly higher nitrogen and phosphorous content. This begins to address the "benefit" part of the definition of carnivory. The higher nutrient content may be an indication of a benefit from the nematodes and the authors note that further investigation, including direct observation of photosynthetic rates, is already underway. More convincing might be an clear increase in biomass or seed set, but with such small plants, elevated photosynthetic rates might be a better measure.

In summary, Philcoxia traps and kills nematodes on subterranean leaves, possibly digests it with enzymes such as phosphatases produced by the plant, absorbs the nutrients, and possibly derives a benefit from the prey in that the plants have higher nutrient content than their noncarnivorous neighbors in the unforgiving and nutrient-poor environment. What's conspicuously missing here is evidence of a lure or attractant. What's the normal concentration of nematodes in the sand surrounding the plant? Is their capture accidental or are they drawn to their death on the subterranean leaves? These questions were also identified by the authors as avenues for further research. I look forward to these!

In my assessment, with further data we can certainly add this genus to the ranks of true carnivorous plants. As Pereira et al. mentioned, this has implications for our understanding of the number of times carnivory has evolved among plants since Philcoxia belongs to the plantain family (Plantaginaceae), which previously counted no known carnivorous plants among its members. Depending on which you include, this means that plant carnivory has evolved at least 7 times independently, a fact I find amazing to ponder.

(h/t to Paul Riddell of the Texas Triffid Ranch for originally pointing me to this new research. Thanks!)

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References:

Pereira, CG, Almenara, DP, Winter, CE, Fritsch, PW, Lambers, H, & Oliveira, RS (2012). Underground leaves of Philcoxia trap and digest nematodes. Proc. Natl. Acad. Sci. USA : 10.1073/pnas.1114199109

Fritsch, PW, Almeda, F, Martins, AB, Cruz, BC, & Estes, D (2007). Rediscovery and Phylogenetic Placement of Philcoxia minensis (Plantaginaceae), with a Test of Carnivory Proc. CA Acad. Sci., 58, 447-467

Taylor, P., Souza, V., Giulietti, A., & Harley, R. (2000). Philcoxia: A New Genus of Scrophulariaceae with Three New Species from Eastern Brazil Kew Bulletin, 55 (1), 155-163 DOI: 10.2307/4117770

The peculiar modification of the locket triggerplants

Cunabulum. If you know your Latin, you might recognize this as "cradle" or "nest." If you do a Google search for it, you'll get a lot of hits for this blog, a few dictionary entries, and a helpful note that wants to know if you meant to search for incunabulum instead. (FYI, incunabulum, according to Wikipedia, refers to a "book, pamphlet, or broadside that was printed - not handwritten - before the year 1501 in Europe." And now you know.) Your search will also probably reveal the orchid species Phloeophila cunabulum, so named because its flower in some ways resembles a cradle. Conspicuously missing from the search results, however, would be the application of this Latin word to an interesting morphological feature of certain species of Stylidium, or triggerplants, a genus of small herbs mostly native to Australia.

Stylidium roseo-alatum - By Jean Hort. (Seriously, go follow her impressive photos on Flickr.)

There are plenty of reasons to be interested in Stylidium. For starters, the genus probably has around 300 species, which makes it the fifth largest genus in Australia. Their variety in color and habit (ephemeral, climber, creeper) is astounding. Did I mention that they may be carnivorous? Most notable of all, perhaps, is the irritable column or "trigger" - the fused male and female reproductive organs that hang beneath the flower and snaps into action, dusting pollinators with pollen when they come for a sip of nectar.

Stylidium debile - An animation of the column resetting after firing; each frame is 1 min.

The complex column, a feature that many plant groups possess combined with the fact that it is one of the faster plant movements in completing its swing in 15 milliseconds is amazing enough. But if you really study this variable genus, you will find diagnostic differences in the morphology of that remarkable column. There's one particular group singled out for its interesting characteristics. I'll let Rica Erickson, the distinguished Western Australian naturalist who passed away just a few years ago at the age of 101, describe this for us:

There is a peculiar in-folding at the apex of the Locket Triggerplant's column. It bends forward into a pouch formed by the dilatation of the column itself. It thus resembles a miniature locket with elastic hinges, enclosing the precious packet of pollen inside the lid. This can be prised apart with a pin to reveal the four neat divisions of the anthers within. ... As the stigma develops it becomes more bulky and no doubt heavy enough to cause the hinge to lose some of its elasticity and at this stage the locket hangs partly open. (Triggerplants, 1958. p. 70.) [Emphasis added]

So, the anthers develop first, then thwack, the trigger deposits pollen on the back of visiting grey-flies. After the pollen is shed, the sticky stigma develops and pushes the anthers out of the way. The plant is now ready to receive pollen from other plants in the same manner that it just parted with its own pollen, a clever evolutionary adaptation to promote cross-fertilization.

Stylidium turbinatum - Column in the set position to the left and beneath the
petals, with prominent stigma and anthers pushed to the side. The "locket" here
is somewhat open, possibly because the stigma is heavier or because of multiple firings.
Source: Holger Hennern.

(I should mention here that a modern interpretation of species that possess a cunabulum by Australian botanist Juliet Wege excludes S. turbinatum, noting that the column is only slightly broadened and a complete cradle for the anthers is not formed; Wege, 2006.) With the above photo of Stylidium turbinatum in mind, let's take a closer look at just the column of a different species, as drawn by another Australian botanist, Allen Lowrie:

Stylidium perizostera column - (Left) Looking down from
above and (right) view from the side. Scale bar = 1 mm.
Original drawing from Lowrie & Kenneally (1997), annotated by me.

At last! The cunabulum is clearly illustrated. This particular species, Stylidium perizostera, has lateral wings on the cunabulum. Most other cunnabula on other locket triggerplant species consist of a simple pouch. Both of the unfamiliar terms in the drawing above, cunnabulum (Latin: cradle) and torosus (Latin: muscular; in Stylidium, the sensitive mobile hinge) were chosen by Kenneally and Lowrie (1994) to be applied to the locket and hinge, respectively. Since then both words have been used only occasionally in this context, so they still remain obscure botanical terms, but they're useful when trying to use these features as diagnostic differences between species. To emphasize the special adaptation of the cunabulum, compare the backside of the widened portion of the column that corresponds to the cunnabulum in Stylidium turbinatum and the slender, smooth column found in other species like Stylidium purpureum.

So... what does it do?

Stylidium preissii - the lizard
triggerplant, also with a cunabulum.
Photo by Jean Hort.

You may be asking yourself, it's a cradle that holds the anthers, so what? Is there any particular function that we can infer from the morphology? Rica Erickson, again:

What is the function of this peculiar modification of the Locket Triggerplant's column? Let us watch. We must stoop very low because the plant grows close to the ground, moreover the trigger is very small. Fortunately the flies are not too wary and we can see them probing. Notice how the column suddenly shoots over. See how the force of the flying trigger flings open the locket. The anthers are held erect and pressed against the fly's shoulder. The insect flies away and swiftly the elastic hinge refolds the anthers again. The trigger has to jerk quickly to swing open the locket.

What then can be the function of the pouch? Does it conserve the moisture of the pollen grains during the dry October heat? Or is it an economical device for saving the loose grains that spill out of the anthers while waiting for insect visitors? That may be the answer, for some pouches retain a little cluster of loose grains near the hinge. (Triggerplants, 1958. p. 70.) [Emphasis added]

After Erickson's initial hypotheses of preventing desiccation or loss prevention of precious pollen, the American botanist Sherwin Carlquist had his own impressions of the locket. One of my personal botanical heros, Carlquist began studying Stylidium species on his trip to Western Australia in 1962 with the aid of Erickson's book which he had found in a Perth bookstore. He returned to Australia several times and identified many new species in his meticulous studies of the Australian flora. In 1969, Carlquist addressed the widened columns or "lockets" mentioned by Erickson. In his assessment, the adaptation "appears to be nothing more or less than a method of achieving self-pollination" (Carlquist, 1969). While Erickson didn't explicitly mention self-pollination, the meaning can be inferred from her suggestion that the cunabulum saves the loose pollen grains, presumably for the stigma to receive.

But as Juliet Wege, the botanist currently working on Stylidium, mentions, many species in this genus have lethal post-zygotic barriers to self-fertilization. That is to say that if pollen from genetically identical individuals is received on the stigma, fertilization occurs but the embryo is aborted and viable seed is not produced. By all accounts, the floral column and trigger mechanism evolved to promote cross-pollination, further supported by the post-zygotic seed abortion found in perennial triggerplants of southern Australia. Wege concludes that, "[i]t is therefore unlikely that the locket has evolved as a self-pollination mechanism in the perennial creeping species..." (Wege, 2006). Wege goes on to explain that tropical annual species, on the other hand, that also have a widened column may have evolved the pouch-like dilation fringed by hairs (papillae) to retain pollen and promote self-fertilization. Annuals, after all, depend on high seed set to survive from year to year.

Stylidium eriopodum - Here just to break up the wall of text. Photo by Jean Hort.

So if the function isn't pollen retention for self-fertilization among the perennial triggerplants from southern Australia, what about the other hypotheses? Erickson's idea that it prevents desiccation of pollen during the hottest and driest months of the season has not received much mention or any data to support or refute it. Wege (2006) throws one more hypothesis into the mix by noting her field observations that pollinators, specifically long-tongued flies, will hover near recently triggered flowers to steal pollen from the anther before it has the chance to reset. Could the cunabulum provide protection from pollen pilferers? It's an attractive idea, but no published data exists.

While we're left wondering what the exact function of a dilated column, pouch, locket, or true cunabulum is, we can also ponder the evolutionary history of the trait. We have widened columns of different varieties from simple to elaborate present in multiple lineages of Stylidium: tropical annuals, creeping perennials, tile-leaf triggerplants like S. preissii, scale-leaf triggerplants, and whorled-leaf triggerplants. Wege is currently working on the phylogeny of the genus, but it's quite clear that this "peculiar modification" has arisen a number of times in the evolutionary history of the genus. I look forward to resolutions of such interesting questions as these.

It is amazing to me how much can be written about, and inferred from, the structure of an morphological adaptation no greater than 3 mm long on the reproductive floral column found on a genus of Australian plants. This is why botany is endlessly fascinating. This is why I love botany.

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References:
Carlquist, Sherwin (1969). Studies in Stylidiaceae: new taxa, field observations, evolutionary tendencies. Aliso, 7, 13-64.

Erickson, Rica (1958). Triggerplants. Paterson Brokensha Pty. Ltd., Perth.

Kenneally, KF, & Lowrie, A (1994). Stylidium costulatum (Stylidiaceae), a new tropical species of triggerplant from the Kimberley, Western Australia and the lectotypification of S. floodii. Nuytsia, 9 (3), 343-349.

Lowrie, A, & Kenneally, KF (1997). Eight new species of triggerplant (Stylidium: Stylidiaceae) from northern Australia. Nuytsia, 11 (2), 199-217.

Wege, J (2006). Taxonomic notes on the locket trigger plants from Stylidium subgenus Tolypangium section Repentes. Nuytsia, 16 (1), 207-220.

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Thanks to Paul of the Texas Triffid Ranch for the recent mention. It provided motivation to finally get around to this overdue post. Cheers!

Is it an insectivorous or carnivorous plant?

When I first read about the Google books Ngram Viewer, which allows you to search its vast archive of digitized books for the proportional usage of different words or phrases and displays the results over time, I immediately searched for "carnivorous plants" to be displayed with "insectivorous plants." (And a note for the uninitiated: the Ngram Viewer is case-sensitive, so while "Insectivorous Plants" and "insectivorous plants" produce similar trends, the title case variant provides the better approximation because of historical usage of title case for this phrase.) I wasn't surprised by what I found.

Peaks and valleys: The Google books Ngram Viewer search I performed. Smoothing = 2.

Frustratingly, the y-axis is unlabeled, but I believe it corresponds to the percentage of all books that the bigrams I chose appear in.

First, a caveat. The limitations of this search are obvious: the results returned are restricted to books in the public domain or ones Google has digitized, there is significant duplication in some of the more popular books that were reprinted multiple times and leads to artificial peaks, and errors in the OCR text can cause problems.

Given all that, though, what can we learn from my search? It would appear that almost no one was using either of these terms to describe flesh-eating plants prior to about 1870. This is consistent with what we know about botanical knowledge from that period. For example, when the Venus flytrap was first discovered and passed around from botanist to botanist, it was mostly an oddity that the less-than-prude educated men of the time giggled at, but there was only little speculation on its function and they didn't have the language to describe it quite yet. It also took decades from its initial discovery for live plant material to reach European botanists.

Enter, of all people, Charles Darwin.

Ready for dinner: Illustration of Dionaea muscipulafrom Darwin's Insectivorous Plants (1875).

With the publication of his book Insectivorous Plants in 1875, the world now had its first excellent experimental evidence to support the idea of flesh-eating plants. Prior to Darwin's treatise, plants native to Europe, such as Drosera (the sundews) and Pinguicula (butterworts) were known to be covered in insects, but that is hardly evidence of carnivory - have you ever taken a look at a tomato? This book can be cited as the reason why the term "Insectivorous Plants" receives such a large boost after 1875 in the graph above.

At the same time, though, "carnivorous plants" was also favored, with both terms receiving similar hits and possible even in the same books. Further Google Scholar searches, unfortunately not indexed by the Ngram Viewer, reveal early 1860s and '70s papers that mention either terms, but none before that. Even the trusty Oxford English Dictionary lists the first mention of "carnivorous" in a botanical context as occurring in 1868 and Sir John Lubbock's 1874 On British Wild Flowers Considered in Relation to Insects as being one of the earlier mentions of "insectivorous plants."

Nepenthes by Drew Avery.

And finally, since about the 1940s, the term insectivorous has fallen out of favor among botanists. This may have been because studies began revealing that many insectivorous plants spend a lot of their time capturing things other than insects, such as spiders. And while the exceptions such as the odd mouse or two found in a Nepenthes pitcher don't matter all that much, for the most part the prey of these plants belong to the broader Arthropod phylum and not the more restricted insect class. To be nit-picky, it's technically correct to call these plants insectivorous, as insects are part of their diet, but that excludes the other organisms they may catch with decent frequency. The broader term carnivorous plant is now perhaps finally replacing the other, though "insectivorous plant" persists to some degree.

For more information on Google's Ngram Viewer, see this TED Talk: What we learned from 5 million books.

Stylidium debile

Stylidium debile F.Muell., a triggerplant from Queensland and New South Wales in Australia, is in near constant bloom in my greenhouse. They bear small, attractive flowers on multiple inflorescences and are easily propagated by cuttings. Of all the Stylidium in cultivation, this is perhaps the most common because it seems to thrive on neglect and tolerates nearly any conditions. For more, see the International Triggerplant Society.

Sarracenia flava var. cuprea

Sarracenia flava var. cuprea, the copper-colored variety of the yellow pitcher plant described by Donald Schnell in 1998. This taxon is the progenitor of several popular copper lid cultivars. The photo was taken at Hortus Botanicus in Leiden during the International Carnivorous Plant Society conference in 2010.

October's Berry Go Round and crowd funding of science

Unexpectedly, I found that my post on protogeocarpy was included in October's Berry Go Round, a blog carnival on plant science, over at Slugyard. Mike B. of Slugyard put the carnival together in a pretty neat way, adapting Poe's "The Raven" for the Halloween edition of the Berry Go Round.

Hyobanche sanguinea, a parasitic plant native to South Africa and the subject of Andi Wolfe's #SciFund project.
Photo source: Winfried Bruenken, Wikimedia Commons.

Unrelated by also interesting, have you noticed all of the opportunities out there for crowd funding a project? Musicians and artists have been ahead of the curve on this trend; for example, I'm supporting the recording of The Guggenheim Grotto's next album over at PledgeMusic. And then there's a multi-year project of one artist seeking support on Kickstarter to complete a beautiful illuminated manuscript of Darwin's On the Origin of Species (h/t Matt Young at Panda'sThumb). So just a few months ago, a few scientists got together and wondered, "Hey! Where are our crowd funding opportunities. Will it work for science?"

You bet it will work! I would encourage you to check out Andi Wolfe's #SciFund project and support it if you can. Andi is a professor in the department of Evolution, Ecology, and Organismal Biology at The Ohio State University that I just began attending this autumn, and the funding from her #SciFund project will support undergraduate research. (Also check our her lab's blog.)

I think overall that the #SciFund challenge will benefit scientists and the public. Scientists must strive to explain often difficult topics to a "why should I care?" public, flexing their PR muscles, and the public gets the opportunity to feel like they're a part of the scientific process. It's exciting and I can't wait to see what comes from it. Good luck, Andi!

Let me rewrite that headline for you...

Arthritic dog lays down for an hour, falls asleep, seems more calm

...or as the New Jersey Herald puts it, "Reiki expert channels energy to heal pets, humans."

No, really. I was shocked. This is journalism? I was also a little embarrassed; this is my hometown newspaper. I always thought it outperformed the newspaper of my adopted hometown, Mount Vernon, Ohio. In my opinion, this was an abominable piece of journalism.

When Cindy Nolte arrived at the home of her client for their afternoon Reiki session, Kodi was waiting for her. Walking with a slight limp because of his severe spinal arthritis, Kodi braved the discomfort to rush to greet her.

The pair walked inside and Kodi lay down on the living room floor as Nolte began to meditate and focus a positive energy flow to Kodi's aching bones and muscles.

Within moments, Kodi's labored breathing had slowed down, and he slowly began to relax into a sleep-like state. Nolte used no words, she didn't even touch Kodi during their hour-long session that seemed to leave Kodi re-energized and invigorated.

I can't believe my hometown newspaper reports this pseudoscience as if it were real, with no disclaimers or editorializing by the journalist that these practices are unproven and frequently mocked by the scientific community. And shame on that woman, Cindy Nolte of Fresh Look on Life, for taking advantage of gullible and desperate people by telling them she can make them (and their pets?) feel better just by thinking at them. Dear lord, just think of the harm she could do if she turned her healing thoughts to murderous ones! (Snake oil, anyone?)

Seriously, though, that this passes muster for journalism (or at best a fluff piece) does not bode well for the journalism profession or the New Jersey Herald. I am sad to say that I've lost respect for the paper.

Acting as a conduit for the flow of positive healing energy, Nolte uses her experience to help her clients quiet their minds and connect to the energy, which can be challenging for busy humans.

"Some people have never tried anything like this before, and trying to quiet their minds after 30 or 40 years is a challenge. Just think of contacting a friend after 30 years; there is a lot to talk about. It's the same for us. We really don't talk to ourselves, so there is a lot of chatter to get through," Nolte said. "We need to learn to go inward and accept ourselves at our own individual level."

Oh. So Cindy Nolte is some sort of life coach that teaches people how to relax. Why not just say that? Why couch the albeit mockable need for a life coach in reiki healing energy woo and weirdness? If you ignore the reiki, this sounds somewhat reasonable. Relaxation is good, and some people are bad at doing it. But she doesn't stop there:

Animals, on the other hand, seem to have a natural understanding of Reiki and the energy it uses to heal, Nolte said. This allows them to benefit from the treatment that the Reiki sessions provide.

Oh. They do? Dear journalist, where's the balance? Actually, screw balance, where is the outright mocking of this pseudoscience? Where's the scientist in the article exposing this practice for the ridiculous assertion that it is with not a shred of evidence to support it? Even a single throwaway line from a local scientist would have been an improvement, though overall the article would still be a loss for those who value logic and reason.

Yes, I realize this article was a slice-of-life in-the-community approach, but it wrongly lends the validity of the newspaper to the laughably irrational tenets of reiki practitioners, who are no more rational in their beliefs than proponents of homeopathy. Unfortunately, people with little knowledge of science could be easily convinced by this charlatan, Cindy Nolte, and her thought energy. I encourage all readers to visit Quackwatch's examination of reiki and this entertaining piece at scienceblogs for a pretty thorough debunking.

I look forward to the next article in the series from the New Jersey Herald on how someone is selling vials of homeopathic "treatments" consisting entirely of water and how it's helping relieve her client's pet opposum's tinnitus. I'm sure Betty the opposum writes excellent testimonials.

Protogeocarpy in the bizarre Australian plant genus Alexgeorgea

Alexgeorgea - male vegetative plant with inflorescences (left), a female vegetative
plant (center), and the above ground portion of the female flower (right), positioned
for the comparison but would normally be shorter. Source: Sherwin Carlquist.

Botanists often love language, so much so that they attach a name to even rare phenomena - odd, tongue-twisting descriptive names that are so infrequently used that one sometimes wonders why they bother at all. Wading into the obscure language of botanists today I encountered this doozie: protogeocarpy. Breaking the term down into its constituent parts gives us proto (before), geo (ground), carpy (relating to the carpel - the ovule and seed producing reproductive organ). Perhaps two-thirds of this word looks familiar to you. The news of the newly described genuflecting geocarpic plant from Brazil, Spigelia genuflexa, has made headlines around the world as a photogenic botanical oddity. I even wrote about it briefly.

Most dictionaries and encyclopedias will tell you that geocarpy is a process by which a plant stem or inflorescence elongates and deposits the developing fruits into the ground. And they will probably mention the famous example of the peanut being buried up to 10 cm below ground. But that's not entirely accurate. Geocarpy is a broad term that encompasses any subterranean ripening of the fruit. Technically, Spigelia genuflexa and peanuts are perfect examples of a type of geocarpy known as hysterocarpy, "in which the fertilized ovary penetrates into the soil by means of a long peduncle," according to the book Dispersal Biology of Desert Plants by Karen van Rheede van Oudtshoorn and Dr. Margaretha W. van Rooyen. In other words, these flowers were fertilized above ground, then the developing fruits were deposited into the soil later. In another twist, only some of the fruits of Spigelia genuflexa were deposited, which the authors of Dispersal Biology would further demarcate as an amphicarpic habit.

The subterranean fruit of Alexgeorgea,
about the size and shape of an acorn.
Source: Sherwin Carlquist.

So in keeping with our geocarpic plant theme, let me introduce the small Australian genus Alexgeorgea. In sharp contrast to the above examples, the three species in this Western Australian genus of restiads (members of the Restionaceae family, related to grasses and sedges) produce their female flowers below ground with all but the stigmas, the pollen-receptive part of the carpel, being subterranean. These are truly protogeocarpic plants because fertilization of the ovary and maturation of the fruit occur below ground.

The male plants (yes, the plants in this genus are dioecious, meaning there are separate male and female plants) of Alexgeorgea nitens appear like many other Australian restiads, so much so that it was first described by the German botanist Christian Gottfried Daniel Nees von Esenbeck in 1846 as Restio nitens. von Esenbeck had mistaken deformed portions of plants above ground, possibly the result of a smut fungus, as the fruit and included this information in his description when placing it in the large genus Restio. Overlooked for the next 130 years were the subterranean fruits of this species until Sherwin Carlquist, an American botanist and one of my botanical heroes, noticed the ephemeral thread-like stigmas of the female flowers emerging from the sand. He admitted that had he not been present during the short period in which the plants produce the female flowers, the peculiar subterranean flowers and fruits would have likely remained unknown to science. Carlquist first came upon these plants in 1974 and later described two species in a new genus named in honor of the Australian botanist Alex George in 1976. Consider how fortuitous this discovery was in not only being in the right place at the right time, but also being able to recognize that the minute above ground portion of the female flower no more 3 cm tall was worthy of further investigation.

Male flowers in the background;
emergent female flower parts seen
in front as red or purple threads.
Source: Sherwin Carlquist.

What you see above and to the right in the photo is a portion of the underground rhizome, which can be several meters long. The female flowers are borne directly on the rhizome 10 to 15 cm below ground in white sandy soils. Overall, Alexgeorgea species are not the most attractive species out there, but they have a certain charm in their unusual habits.

But why? What conditions lead to the evolution of geocarpy? What are the advantages? Carlquist hypothesized that in Alexgeorgea the evolution of a single-seeded subterranean fruit was an adaptation in response to a predominant fire ecology in Western Australia. Fruits at or below ground are protected from the extreme heat of fire. Indeed, many other plants in Western Australia have adapted to frequent fires by producing their fruits at ground level (basicarpy). More widely, geocarpy is assumed to have evolved in several plant lineages in response to the harsh environments in which the species grows. In Dispersal Biology of Desert Plants, it is noted that plants may develop a geocarpic habit to ensure close proximity of the offspring in favorable micro-habitats. For example, Alexgeorgea persists in seasonally wet peaty sand and if it instead relied on wind dispersal of its fruit, it is assumed that a larger percentage of offspring would fail to germinate in favorable soils by being blown far from the small region in which it can thrive. The disadvantages are obvious: restriction of seed dispersal, limitation of population genetic structure, and the possibility of small stochastic events wiping out entire colonies.

Regardless, this is a fascinating plant habit and an equally fascinating genus. Leave it to Australia to bring us yet another botanical oddity!

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References:

Carlquist, S. (1976). Alexgeorgea, a bizarre new genus of Restionaceae from Western Australia.
Australian Journal of Botany, 24 (2), 281-295 DOI: 10.1071/BT9760281

Briggs, B., Johnson, L., & Krauss, S. (1990). The species of Alexgeorgea, a Western Australian genus of the Restionaceae. Australian Systematic Botany, 3 (4), 751-758 DOI: 10.1071/SB9900751

Spigelia genuflexa: You reap what you sow

Spigelia genuflexa leaning over to deposit its seed in the soft soil. Photo by Alex Popovkin (CC by 2.0)

If you haven't yet checked out the beautiful photos of this newly described species, definitely do so. Spigelia genuflexa Popovkin & Struwe is a member of the Loganiaceae, or strychnine family, just described yesterday in the journal PhytoKeys. It is unusual in the family by its geocarpic habit; I'll let Alex Popovkin and his co-authors explain:

During fruit maturation, the basal infructescences bend down towards the ground, depositing the fruit on the surface (and burying it in soft kinds of ground cover, e.g., moss), whereas the upper ones do so slightly but noticeably.

This plant clearly doesn't trust that gravity will do the job appropriately. A geocarpic habit is rare but common enough to have representatives in several families. The most interesting to me about this story is that the first author of the study and one of the authors of the taxon is an amateur botanist in Brazil whose efforts have paid off. And as an aside, the guest editor for Popovkin's paper was Sandra Knapp, the botanist I mentioned earlier who was instrumental in successfully altering the botanical nomenclature code to allow online publication of new taxa.

ScienceDaily published a decent press release on this new species and the University of British Columbia's Botany Photo of the Day provided an excellent summary. (I highly recommend adding the Botany Photo of the Day site to your RSS feed.)