The carnivorous plant with catapult traps

Drosera glanduligera (pimpernel sundew) shown here in a figure from the
new paper describing the fast-acting catapult traps (Poppinga et al., 2012).
Creative Commons Attribution License.

As usual, I'm late to the party and many other outlets have already written about this fascinating new paper published in PLoS ONE; such is the nature of the captivating world of carnivorous plant research. I'll try to place the new article in a bit more context.

First, the study organism: Drosera glanduligera, the pimpernel sundew, an Australian native, was first described in 1844 by Johann Georg Christian Lehmann who was cataloging and describing new species found in the collections of the botanical garden that he established and directed in Hamburg (now called Alter Botanischer Garten Hamburg). My botanical Latin needs a good refresher, but at a quick glance it appears to me that Lehmann noticed enough to write down that the marginal tentacles of this species are larger, but that's the only observation he recorded. Indeed, as you can see in the photo above, the marginal tentacles are much longer than the glue-tentacles closer to the center of the leaf lamina (more on this later).

Drosera regia, king sundew.
My plant in cultivation.

It turns out that, at least with this species, nothing more was recorded on what is apparently a fascinating trapping mechanism more analogous to the fast snap trap action of the Venus flytrap swiftly snatching a meal as seen here. That is until Richard Davion began making new field observations in 1974 when he wasn't even ten years old yet and published them in the 1990s in the relatively low circulation newsletter of the Carnivorous Plant Society of New South Wales. This underscores the importance of publishing new observations in journals where your work might get noticed. Davion later contacted two authors of the current study, the Hartmeyers, in 2003 and asked them to corroborate his findings. Within two years they confirmed Davion's observations and presented a film titled, "Drosera: Snap-Tentacles and Runway Lights," at the International Carnivorous Plant Society conference in 2006 that summarized their findings. (The video can be seen in full on YouTube courtesy of the ICPS.)

Snap tentacles: Everyone is excited about this research - and rightly so - but what exactly are snap tentacles and how do they differ from regular tentacles on sundews? On most sundew species like this Drosera regia above and to the right, there is one kind of tentacle: a few-celled stalk supporting a multicellular, glandular, globular head. They vary in length from the center to the edge of the leaf but not in overall morphology. They produce and rely on a viscous mucilage to retain captured prey until the tentacles slowly move (in some species, if at all) and direct the prey toward the digestive glands at the center of the lamina. This can take minutes, even half an hour depending on temperature. The snap tentacles, on the other hand, produce no mucilage and typically have a faster movement. The multicellular head is modified and looks more like a spatula or a pillow resting on oversized spoon (or maybe like a catapult?). They quickly flip unsuspecting prey up and into the center of the remarkably sticky mucilage produced by other tentacles. In milliseconds the prey can reach a maximum velocity of 0.17 m/s and a maximum acceleration of 7.98 m/s. Before it can think or react, it's deposited in the lamina where it's immobilized and often suffocated by the mucilage. Any struggling is futile as other slower tentacles reposition the prey nearer the digestive glands. A few days later after the plant's enzymes have done their work, meal time is complete and new leaves are unfurling, awaiting new dinner guests.

About two years ago, two of the authors of the current study, Siggi and Irmgard Hartmeyer, published their findings on over 100 Drosera taxa in the Carnivorous Plant Newsletter while investigating snap tentacle morphology. They concluded that many species of Drosera from multiple points on the established phylogeny of the genus have snap tentacles of some kind at some point in their ontogeny that vary in how swift the response is. It's important to note, however, that in the 2010 paper they set aside the tentacles of Drosera glanduligera as something wholly different since it was the fastest and the mechanism wasn't quite clear. This may be the reason why we can refer broadly to snap tentacles and flypaper traps on all the species but this one alone has been granted the new term catapult-flypaper-trap.

For their part of the new study, Irmgard and Siggi cultivated the plants, captured new HD film, and created this documentary to accompany the paper's release. Now this is effective science communication (in German with captions in English). If you want to skip the beginning and see the plant in action, make your way to about the 5:00 mark.

So that's cool! A catapult that helps deliver prey in the center of the trap. What else did they find? I'm glad you asked. These tentacles move by some pretty awesome mechanisms since they're moving so quickly - did you watch the video? It completes that swing from laying on the ground to delivering the prey to the hungry center of the leaf in as little as 75 milliseconds. In their investigation, the research team found that these snap tentacles actually deform beyond the ability to "reset" in a resting position to fire once again like the Venus flytrap can. They hypothesize that the cells in the hinge zone actually buckle from the stress involved with the movement - nature's one use only device.

In the discussion, they spend a good bit of real estate on hypothesizing on the mechanism involved: is it rapid water movement from one side of the tentacle to the other or loss of turgor pressure in combination with what would essentially be the release of stored potential energy by a sudden geometric change or curvature inversion not unlike this child's toy (oh, you know you remember annoying your parents with one of those.) But they didn't find any noticeable inversion. This may not be all that different from other tentacle movement (and the initiation of movement in the Venus flytrap) where the acid growth hypothesis is supported. Simply, in acid growth a signal would cause H+ ions to be pumped out of the cell into the cell wall space where proteins in the cell wall matrix known as expansins loosen at an acidic pH (higher H+ concentration). That allows the cells to increase in size very rapidly. If you do this on only one side of the tentacle, the lower surface, the result would be rapid bending inward. There are ways to inhibit the transporters associated with acid growth, but it might take the skills of a fine surgeon to delicately and strategically place the inhibitors on the tentacles without prematurely triggering them!

Regardless, there are plenty of possibilities here for future research, much of which was identified by the authors themselves in the last few paragraphs. Congratulations all around for such an attention-grabbing paper that was even blamed, in part, for slowing down the PLOS website:

Ha! Our site slowdown blamed on mega-popularity of PLOSONE's carnivorous plant bit.ly/RlVHLu and Cannibis papers bit.ly/S3Oy53
— PLOS (@PLOS) September 27, 2012

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References:
Poppinga, Simon, Siegfried R. H. Hartmeyer, Robin Seidel, Tom Masselter, Irmgard Hartmeyer, & Thomas Speck (2012). Catapulting Tentacles in a Sticky Carnivorous Plant. PLoS ONE, 7 (9): e45735. 10.1371/journal.pone.0045735

Hartmeyer, Irmgard, & Siegfried R. H. Hartmeyer (2010). Snap-tentacles and runway lights: summary of comparative examination of Drosera tentacles. Carnivorous Plant Newsletter, 39 (4), 101-113.

Oeceoclades gracillima: won't you crawl inside?

Don't you just want to crawl inside?

Oeceoclades gracillima (Schltr.) Garay & P.Taylor is an orchid native to Madagascar that has stunning maroon and black mottled foliage which is hard to capture properly on film, but you can see one of the better images here. (In case you were wondering, you pronounce the genus name ee-see-o-CLA-deez.)

I picked this one up from Michel Orchid Nursery when they were at the orchid show and sale at Longwood Gardens in March 2012. I'm so happy it finally flowered as this means I'm able to dry and press a specimen for a voucher and begin working on isolating and sequencing DNA from the leaves and flowers on the other inflorescence. It's not the prettiest flowering orchid around - the flowers are mostly small and drab - but it's got character elsewhere in the leaves.

For those of you with a sharp eye who follow the blog because of my interest in carnivorous plants, you'll notice that this species had originally been named Eulophia gracillima by the German orchid specialist Friedrich Richard Rudolf Schlechter in 1913. That name was supplanted in 1976, however, by the new combination when Leslie Andrew Garay and none other than the Utricularia expert Peter Taylor!

Taylor was also the co-author of another combination, Oeceoclades roseo-variegata, which according to the Kew World Checklist is now a synonym of O. gracillima. The former is still in use, however, and was how my plant came labeled from the nursery.

Beauty is in the eye of the beholder, I suppose, and this little flower has a wonderful little nectar spur. Overall, a great, compact orchid that was really easy to cultivate.

Tweeting the 9th biennial International Carnivorous Plant Society conference

Participants browsing the sales area at the 8th ICPS conference (2010) in Leiden, Netherlands. Photo by kitkor.

At the end of the week I'll be on my way to my second International Carnivorous Plant Society conference, the last being held two years ago in Leiden, Netherlands. (When they said International, they meant it.) It's a relatively convenient trip from Ohio to Seekonk, Massachusetts where the New England Carnivorous Plant Society will host the international conference, the first time it's been back in North America since 2006.

Unless there are unforeseen technical difficulties, I plan to tweet along with the presentations, just like I did for several of the Botany 2012 sessions I attended. If you're so inclined, you can follow me on Twitter where I'll be using the hashtag #ICPS12 if anyone else wants to join in (#ICPS2012 was already taken by a few recent tweets on a physics conference). I've also made a resolution to do a better job at updating the blog during the conference, but of course this may prove to be difficult.

It will be great to see so many colleagues and friends, especially those I've known only through our weekly Board meeting chats via Skype for the North American Sarracenia Conservancy. I'll finally be able to meet many of you in person!

Get ready for some awesome carnivorous plant content fed into your social media.

Peer-review system failed in controversial gay parenting study

In early June a new social science study was published online ahead of print on the purported differences in children who were raised by gay parents as opposed to those raised by heterosexual parents ("How different are the adult children of parents who have same-sex relationships? Findings from the New Family Structures Study" by Mark Regnerus). Concerns were immediately raised about the study's sample, methodology, analysis, and therefore results. Most notably, the study characterized anyone who ever had a same-sex relationship after having a child as thereafter a gay father or lesbian mother regardless of whether they parented the child together as a couple. If you're studying the effects of same-sex relationships on the rearing of children, don't you think this would be an important detail to pay close attention to? This is just bad science.

And a new review by the journal that published the piece agrees. The editor of the journal assigned a member of the journal's editorial board to assess how such a "bullshit" paper got published in the first place. Where did our system break down? The report and the piece in The Chronicle of Higher Education is fairly damning and underscores how important our job as scientists is when we put on our reviewer hats:

In his audit, he writes that the peer-review system failed because of “both ideology and inattention” on the part of the reviewers (three of the six reviewers, according to Sherkat, are on record as opposing same-sex marriage). What’s more, he writes that the reviewers were “not without some connection to Regnerus,” and suggests that those ties influenced their reviews.

I've not yet been asked to put a reviewer's hat on - nor should I until I'm further along in my studies - but I've seen a few publications through the review process and I've seen my PIs, good, thoughtful PIs, calmly refuse to accept manuscripts because of conflicts of interest. I know it's tough sometimes; the academic nature of science is incestuous and we collaborate or have connections with just about everyone in our narrow fields who is qualified to give our manuscripts a thorough review. Or at least that's how it feels sometimes. But that's no excuse. If you're asked to review a manuscript of an author with whom you have a conflict of interest, kindly refuse to accept, simple as that.

In reality, only two respondents lived with a lesbian couple for their entire childhoods, and most did not live with lesbian or gay parents for long periods, if at all. The information about how parents are labeled is in the paper. Regnerus writes that he chose those labels for “the sake of brevity and to avoid entanglement in interminable debates about fixed or fluid orientations.” Sherkat, however, called the presentation of the data “extremely misleading.” Writes Sherkat: “Reviewers uniformly downplayed or ignored the fact that the study did not examine children of identifiably gay and lesbian parents, and none of the reviewers noticed that the marketing-research data were inappropriate for a top-tier social-scientific journal.” [emphasis mine]

And I suppose this is where it all comes down to: flawed peer-review in this case failed to identify severely flawed social science.

Thecostele alata wants to give you a hug

I received this cute little orchid from Gines Orchids last week for my research on genera allied to Dipodium and Cymbidium. Like most species in this group of orchids, Thecostele alata (above) is native to Southeast Asia. Those two slender upper petals sort of look like they're reaching out to give you a hug, don't they? And is it just me or does the column resemble the head of a floppy-eared dog (at least from this angle)? Perhaps I've been staring at this for too long.

New study on carnivorous plants makes headline writers batty

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Before we get started, let me say that I forgive those who write headlines like pollution makes carnivorous plants go vegetarian and carnivorous plants go vegetarian in response to pollution and new study finds that pollution turns carnivorous plants into vegetarians. They know not what they do. It's also tempting to go after the flashy, attention-grabbing headline. Just try to do a better job next time, ok? And while we're on the topic, let us thank those that presented reasonable titles, like the one by Liat Clark at Wired.co.uk: carnivorous plants capture less prey in polluted bogs. Thank you for getting it a bit better! It would also be a terrible oversight if I neglected to mention that the Southern Fried Scientist took this issue to task a few days ago. Bravo!

So, on to the science at hand. What's all the fuss about?

Drosera rotundifolia at Triangle Lake Bog, Ohio. Photo by kitkor.

Drosera rotundifolia, the round-leaved sundew. Or common sundew. Or "bloody hell that thing is everywhere." And it is: North America, Europe, Asia... Here in Ohio it is the most common species of Drosera that you'll bump into - the other being Drosera intermedia, but several sites it had been known from have now been developed. For those unfamiliar with carnivorous plants, you might be peripherally aware that it is thought that these species have evolved in nutrient-poor environments. Given this idea and our knowledge that most species possess a good deal of phenotypic plasticity in response to environmental cues, researchers decided to further test earlier experimental observations that Drosera rotundifolia reduced its investment in carnivory (as measured by stickiness in units of force used to remove a piece of filter paper from the leaf) when grown in the presence of more nitrogen (Thorén et al., 2003).

Here in the new study, the researchers, a team including J. Millett of Loughborough University, B. M. Svensson and H. Rydin of Uppsala University, and J. Newton of the Scottish University Environmental Research Centre, were more interested in the relative amount of nitrogen that came from prey captured by normal means and from the roots as a result of increased nitrogen available from atmospheric deposition due to increased air pollution.

Briefly, the authors identified three bogs in Sweden that represented a gradient of mostly pristine to somewhat polluted in terms of nitrogen deposition. Fifteen specimens were removed from the bogs, dried, and analyzed for stable isotopes of nitrogen. Once they had their isotope data, all they did was subtract surrounding Sphagnum isotope data from Drosera and divide that by (insect - Sphagnum), where insect represents the mean isotope number for prey captured on the plant at the time of collection. And there's an easy ratio!

So conclusions from this? Well, the authors state it very clearly in the abstract, which many of the headline writers must have missed: "Drosera rotundifolia plants in this study switched from reliance on prey N to reliance on root-derived N as a result of increasing N availability from atmospheric N deposition." (emphasis mine) No, headline writers, these plants were not "OMG BECOMING VEGETARIANS!" Wouldn't that be a plant eating plant matter? And, as strange and wonderful as nature is, we have two possible examples in Nepenthes ampullaria and Utricularia purpurea where the former seems well-adapted to catch leaf litter and the latter appears to primarily cultivate algae in its bladder-like aquatic traps. No, dear headline writers, increased pollution will not turn Drosera rotundifolia into a vegetarian. It may, however, given this work and that before it, be the cause of changing priorities in nitrogen uptake from primarily prey-derived to primarily root-derived. It should be noted, however, that the authors did not set out to assess prey capture rates in these areas, so any statement has to be carefully worded and specifically related to nitrogen assimilation from different sources. We don't know if the plants in areas with more nitrogen capture fewer arthropods. It's entirely possible that the plants that incorporate more nitrogen from their roots capture the same number of prey but preferentially assimilate the nitrogen from the roots.

More troubling, however, is that with increased nitrogen availability in these once off-limits landscapes, opportunistic species may find it easier to overcrowd the poor little perennial carnivorous herbs. (Of course, the increase in nitrogen in this study was not very large and probably would not be enough to allow non-bog-adapted species to thrive.) Most carnivorous plants are low to the ground and depend on high light conditions to thrive; if shaded too much, they may soon succumb to succession. Of course this is only a hypothesis and needs to be studied! I wonder what the headline writers will say then...

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References

Millett, J., Svensson, B., Newton, J., & Rydin, H. (2012). Reliance on prey-derived nitrogen by the carnivorous plant Drosera rotundifolia decreases with increasing nitrogen deposition New Phytologist, 195 (1), 182-188 DOI: 10.1111/j.1469-8137.2012.04139.x

Thoren, L., Tuomi, J., Kamarainen, T., & Laine, K. (2003). Resource availability affects investment in carnivory in Drosera rotundifolia New Phytologist, 159 (2), 507-511 DOI: 10.1046/j.1469-8137.2003.00816.x

A sundew makes a hasty retreat

I'm not yet ready to send out the heralds and call this a success on my first go at cultivating tuberous sundews, but I'm closer now than I was before. If you recall, I originally purchased a lovely specimen of Drosera peltata from California Carnivores in January 2012 and first posted about it in March. It started out as a cute little rosette of carnivorous leaves, then bolted to produce two lovely 6-inch tall stems bearing those irresistible peltate leaves. And then throughout the last few months it was happily going about the business of, well, what sundews do best: capturing prey to collect nutrients.

Most of the tuberous sundews are native to Australia where the winter is rainy and the summer is hot and dry as a bone. This lineage of sundews has evolved the handy adaptation of giving up trying to survive as a full-fledged leafy herb during that hot, dry, unforgiving summer. Instead, they retreat into the soil, packing up their nutrients into root structures called tubers, not unlike a potato in many ways though much smaller.

In just the last few weeks as we approach the hottest late May and early June weather in the Northern Hemisphere here in Ohio, this particular specimen I had was finally ready to make its scheduled retreat. The leaves and stem quickly browned from the tips in a matter of days, my cue to stop watering and let the soil go bone dry lest the tubers succumb to rot as they form. And then, a few weeks later, out of curiosity and because I knew the soil surface in the pot was much too hard for the new growth to break through next year, I dug through the soil to find the tiny tubers:

Those little cream-colored pearls are definitely not perlite! A closer look:

In the above photo, the two tubers toward the top were still attached to the root, the dark brown object leading from center to the bottom right. It was a bumper crop! After sifting through the remainder of the soil, I found ten tubers in all:

The next challenge will be keeping them in a nice, dark place until next fall when they begin to stir. I think the hardest part will be remembering that I have them stuffed away somewhere!

And also, thanks to my friends at Botanical Oddities, I now have tubers from Drosera auriculata. Thanks, guys! Here's hoping I have success with both as I imagine the difficulties of growing tuberous sundews arise when preparing the new soil mix - the sand can't be too sharp or the new growth will be torn up on its several inch ascent from below. It will, at least, be a fun challenge.

Drosera peltata bit off more than it could chew

I found this grisly scene out in the greenhouse when I got home today. It looks like my Drosera peltata got a little overzealous, trapping this fly (ID? I'm hopeless at identifying anything with legs) by the head. It's at the end of this tuberous sundew's growing season, so all of that energy derived from this meal will be going directly to the tuber that should be forming several centimeters below the soil.

Drosera - Reach out and touch someone grab someone by the head.

Go read: Asking permission

Evolutionary biologist Jeremy Yoder who blogs over at Denim and Tweed just posted what I consider to be one of the best narratives of a volunteer for a campaign to defeat one of these repugnant state constitutional amendments that would ban same-sex marriage, this one in Minnesota. He recounts some of his experiences and conversations with Minnesotans who, as he says, are capable of being "astonishingly, densely homophobic, even when they're being Minnesota nice." It's worth the full read.

Ohio may have it's own gay marriage battle brewing, but possibly not until next year. Ballot language was just approved last week so that the Freedom to Marry Coalition is allowed to begin circulating petitions, hopefully gathering the 385,253 valid signatures needed for the issue to be placed before the voters on the November 2013 ballot. Why use the ballot initiative when it seems like an uphill battle? Well, the only way to allow gay marriage would be to repeal the constitutional amendment passed in 2004.

In 2004 62% of Ohioans voted in favor of enshrining discrimination in our state's constitution by banning same-sex marriages and civil unions. It has often been cited as one of the most restrictive amendments in the nation. It reads:

Only a union between one man and one woman may be a marriage valid in or recognized by this state and its political subdivisions. This state and its political subdivisions shall not create or recognize a legal status for relationships of unmarried individuals that intends to approximate the design, qualities, significance or effect of marriage.

A 2006 analysis on the effects of marriage equality on children reported in the journal Pediatrics by James G. Pawelski et al. notes the following on the Ohio law:

As a result, judges around the state have dismissed or reduced charges in domestic violence cases, because Ohio's domestic violence law recognizes the relationship between an unmarried offender and victim as one “approximating the significance or effect of marriage,” thereby representing a direct conflict with the amendment's prohibition against such recognition, thus rendering it unenforceable. [Their reference was this Cincinnati Post article]

 It's clear that the language of the 2004 amendment, specificially "legal status ... that intends to approximate...", has caused the most problems. This can be interpreted widely to include any contract my partner and I create that would "approximate" the qualities normally attributed to marriage. What exactly does this mean? It could be a will, or a private contract, or a medical directive like a power of attorney. And some judges have clearly taken it to mean unmarried partners in domestic violence cases do not require the same protections as married ones.

Unknown to the authors of the cited study above, Municipal Judge Paul Spurgeon of Mount Vernon, my adopted hometown since 2007, went so far as to deny several temporary protection orders in domestic violence cases, often a very necessary and important step regardless of the sexual orientation of those involved, based on his belief that granting temporary protection under the "person living as a spouse" condition would mean recognition of same-sex marriage. Motion denied. (I'm honestly surprised there wasn't more outrage over this.)

I guess the point is that this law is doing real harm and causing a fair amount of chaos in some court proceedings related to domestic violence. But... the effort to repeal the ban and replace it with one that allows marriage faces its own chaos. Apparently, not all organizations are on board and the focus is split, with critics suggesting we should put our energy into obtaining housing and employment nondiscrimination rights first. ("No state has passed gay marriage that has not first had protections in housing and employment," or so I heard on NPR this morning.) And then there's the local perspective. Rick Santorum won my county's Republican primary, but I do have hope that the pendulum is slowly swinging the other direction. This local news story from Marietta, a small town on the Ohio River in Southeast Ohio not known for being liberal got the opinion of four locals. The only dissenting voice was, naturally, from the Catholic priest. The others, ages 19 to 42, said they support the measure and that it didn't matter to them if gay people can get married or not. I'm not sure if the petition efforts will amount to anything and then if the general public will actually vote for the measure in 2013, but, inspired by others, I might put in my own volunteer time.

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Pawelski, J. (2006). The Effects of Marriage, Civil Union, and Domestic Partnership Laws on the Health and Well-being of Children PEDIATRICS, 118 (1), 349-364 DOI: 10.1542/peds.2006-1279

The shield sundew

Encouraged by a Facebook post from California Carnivores and on a whim I decided to get my first tuberous sundew a few months ago. These are plants with a decidedly curious habit unfamiliar to those of us where winter normally equals dormancy. During the winter, more accurately described as the wet season, the plant will spring up out of the soil and produce first a flat rosette of leaves and then begin to bolt, sometimes attaining a height of 50 cm. Once the high heat normally associated with the Australian dry season arrives, the plant withers and retreats to a tuber some 4 to 6 cm underground. I suppose this unfamiliar habit is the reason why tuberous sundews get the reputation of being quite difficult to maintain - they must be kept wet but not soaked in the winter and nearly bone dry in the summer. Luckily, California Carnivores occasionally stocks Drosera peltata, the shield sundew, so named for the shield-shaped leaves, reportedly one of the easiest tuberous sundews to grow. A beginner's plant, if you will.

So far, I'm thrilled with it! I just hope that I'm able to keep the tuber viable through the summer.

As a bonus, I also received the above dainty flowering plant, Utricularia bisquamata. Known as a prolific weed of the carnivorous plant world, I'm not sure if I should torch it or try to contain it. If I don't do something, it is nearly guaranteed that it will end up taking over every single pot in my collection.

Berry Go Round #49

Oops. Looks like I've been neglecting the link-back duty. At the end of February, Bora Zivkovic over at A Blog Around The Clock posted the results of all submissions from February botany-related posts. Among the gems this month were not one but two (Elizabeth Preston and Ed Yong, respectively) discussions of the news that scientists were successful in resurrecting a living plant from seed tissue hidden away by squirrels 30,000 years ago. And then there's the provocatively-titled Are Sheep Better at Botany than the US Government? by Jason G. Goldman of The Thoughtful Animal. And you must not miss the wonderful post by Colin Beale, The paradox of the prickly: Why grow thorns if they don't work? at one of my favorite group blogs, Nothing in Biology Makes Sense! And for the chemically-minded, there's a great post by Andrea Wills titled, Why "Natural" isn't always better: almond extract and cyanide.

Well, you get the point. Go check them all out! And if you have any plant-related posts, consider submitting them or nominating someone else's for the March compilation, which will be hosted by Greg Laden over at ScienceBlogs.

The orchid that smells like Chanel No 5

Dipodium roseum, a parasitic Australian relative. Photo by Ian Sutton.

The orchid genus Dipodium, collectively known as the hyacinth orchids, includes somewhere between 20 to 30 species native to Southeast Asia and Australia. Interestingly, the majority of the species are leafy epiphytes - well, terrestrials that climb and then become epiphytes - dispersed throughout Southeast Asia. A small group of these plants, however, have lost the leaves entirely and live as terrestrial parasites at the base of Eucalyptus trees in Australia.

This, of course, is interesting on its own, but what caught my attention today was the description of a new species in 2006 by Peter O'Byrne and Jaap Vermeulen. They found Dipodium fragrans growing in eastern Johor state of Peninsular Malaysia, inhabiting the lowland swamp-forests common to the area. Dipodium fragrans, as you can deduce from the species epithet, is heavily perfumed, so much so that it led to this humorous description, hidden away among the often stuffy and sometimes inaccessible language of academic botany:

D. fragrans is noteworthy in two other respects: the inflorescence is often branched, and the flowers are strongly fragrant, hence the specific name. Vermeulen describes the scent as "being like Chanel No 5", while O'Byrne (a poor schoolteacher) is ignorant about luxury fragrances and likens the scent to frangipani's.

Science, including the scientific descriptions of  new species, could learn a lesson from O'Byrne and Vermeulen. A little humor, properly placed, makes for a more engaging read. It certainly stuck with me more than if that comment had been omitted!

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Reference:

O'Byrne, Peter, and Jaap Vermeulen (2006). Two Cheirostylis species and a new Dipodium. Malayan Orchid Review, 40, 91-94

Fairy aprons

This plant was given to me by Douglas Darnowski identified as Utricularia paulineae, a beautiful species of bladderwort from southwest Western Australia described by Allen Lowrie in 1998 and named in honor of his wife. However, now that it has flowered, I believe this to be a specimen of the variable Australasian species Utricularia dichotoma (the lower corolla lip is not nearly reniform enough to be U. paulineae), commonly called fairy aprons. Isn't that precious? The small size of these flowers - no larger than your pinky fingernail - and the ruffles certainly fit the common name perfectly. And those colors! Brilliant violet with a neon yellow landing guide.

Carnival of Evolution #44

The newest edition of the Carnival of Evolution, this month's writings on evolution from the busy denizens of science blogosphere, is up at The Atavism. As always, I'm impressed by the work of Carl Zimmer, this time on ion pumps in fungi. Also interesting are the posts "How the cricket lost its song" and another on how extinction isn't always, well, extinction. Even my earlier post on triggerplant morphology was chosen. Got some free time and feel like a little bit of science today? Go check out all the links!

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.