Cunabulum

Fairy aprons

2012-02-14T15:25:00.000-05:00

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

2012-02-02T14:39:00.000-05:00

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

2012-01-30T20:27:00.000-05:00

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

2012-01-09T22:00:00.000-05:00

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!)

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

2012-01-08T16:28:00.000-05:00

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.

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.

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?

2012-01-04T18:33:00.000-05:00

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

2011-12-20T21:45:00.000-05:00

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

2011-11-18T22:36:00.001-05:00

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

2011-11-13T22:41:00.001-05:00

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...

2011-10-31T23:25:00.000-04:00

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

2011-10-02T22:48:00.000-04:00

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!

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

2011-09-15T23:13:00.000-04:00

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.)

Fabulous news: Nepenthes thorelii has been rediscovered

2011-08-07T19:31:00.000-04:00

Time to celebrate! Botanist François Mey has confirmed that Nepenthes thorelii, a tropical pitcher plant native to Vietnam, has been rediscovered. This species was first collected in the mid-1800s, then formally named in 1909, but has most recently only been known from the earlier herbarium specimens. All specimens in cultivation that were labeled N. thorelii were revealed to be related, but did not share key morphological characteristics with the type specimens of the species. And so, it was thought that N. thorelii could have been extinct both in the wild and in cultivation.

Then, in 2009, thoreliigate happened. Vietnamese growers uploaded photos to one of the carnivorous plant forums, showing them holding plants that François identified as true N. thorelii. At one point, the Vietnamese growers refused to cooperate further. When François and other experts searched for the plants at the type location and in the exact spot of the photos, no plants matching the description of N. thorelii were located. It's really quite sad as these plants were clearly poached and sold.

But now François, along with botanist Alastair Robinson, is back in Vietnam and has successfully rediscovered a population of N. thorelii. As Alastair notes, this is the first time in 102 years that qualified botanists have been able to see the plants in situ and collect proper herbarium specimens. Their initial reports and some beautiful photographs can be found here. According to the comments in the forum posts, there are about 100 plants of both genders at this site, located on military land, so chances are that it will remain protected.

Congratulations to all involved! Work like this is very valuable in conservation and taxonomy. Truly fabulous news.

The great golden digger wasp returns!

2011-07-26T22:26:00.000-04:00

The great golden digger wasps (Sphex ichneumoneus), which I wrote about in a post last year on free will and the Concorde fallacy, returned this year to the same spot in front of Higley Hall at Kenyon College in the soft, gravelly soils under an overhang. A swarm of dedicated females has been entertaining our equally dedicated summer science students and visitors. The nest site is conveniently right outside large floor-to-ceiling windows, perfect for viewing the activity of this wasp species. Their short lives will come to an end soon, but they have been able to dig, provision, and complete dozens of burrows. Brava, wasps. I hope this site remains popular for the species for years to come.

Botanists vote to allow online publication of new taxa

2011-07-21T22:36:00.000-04:00

The excitement (and nervous uncertainty) is tangible on botanical taxonomy e-mail lists with the recent news that the nomenclature section of the International Botanical Congress, the governing body of the rules on how we describe new species and other taxa, voted at this year's Melbourne conference to drop the requirement that all new taxa must be described in print publications. If the rule is adopted by the whole Congress, we'll soon see new taxa being published in online-only peer-reviewed journals like PLoS ONE.

Much of the discussion on online-publishing has surrounded the necessity for proper archiving and a sense of permanence on an otherwise ephemeral online realm where the paradox that full permanence may not be achievable yet it's hard to completely erase some online substance reigns. Last year Sandra Knapp of London's Natural History Museum took this outdated policy to task and defiantly published four new species of Solanum in PLoS ONE. She was able to skirt the printed publication requirement by following the other International Code of Botanical Nomenclature rules that allowed her to print out at least 10 copies and distribute them to libraries and a central name index. If the full IBC follows suit and votes for this new rule allowing online publication of new species, no one will have to follow Knapp's example.

This issue had come up at the last Congress in Vienna six years ago, but online journals were just getting off the ground and archiving systems were either poorly managed or lacking entirely. Heck, I was still using Livejournal. A lot has changed in the past six years. The measure didn't pass in Vienna, which I think was the right decision. We waited long enough that the technology caught up to meet the rigorous demands of proper taxon description.

Levenhookia murfetii from Mount Lesueur, Western Australia
Lowrie A, and Conran JG. 2011. Triggerplant Journal 1 (2): 4-29.

In a related matter, I recently noticed that noted Australian botanist Allen Lowrie, famous for his carnivorous plant descriptions, has described a new species of stylewort (Levenhookia) in the online-only Triggerplant Journal (Volume 1, Number 2), founded by Douglas Darnowski and Greg Bourke. It's beautifully illustrated with lovely photos, but as far as I can tell, and even though the journal has an ISSN, the description by Lowrie and his colleague John G. Conran of the new species Levenhookia murfetii (named in honor of Denzel E. Murfet) is not "effective" yet. And so until the new rules from the IBC go into force, all publications of new taxa should still be in print, or at the very least Lowrie and Conran need to print out ten copies of their article from the journal and submit it to libraries and one index, just as Sandra Knapp did with her Solanum species. It may be early to judge based on this, but so far the name Levenhookia murfetii has not been entered into the International Plant Names Index.

Update (27 July 2011): I recently heard from Greg Bourke, one of the publishers of the Triggerplant Journal, that the description of the new species Levenhookia murfetii was indeed printed out and distributed to validate the description. This is good news for this particular description. Perhaps IPNI is just behind on updating the database.

Now the zoologists can sit back and be jealous of the botanists, since the ICBN's zoological counterpart, the International Code of Zoological Nomenclature, has been considering such an amendment to their rules since 2008 but it has not yet taken any action. I'm okay with this.

Lowrie, A., & Conran, J.G. (2011). An overview of the Australian Levenhookia (Stylidiaceae) complex, including a new species (L. murfetii) and observations on the triggering methods employed for pollination and outcrossing. Triggerplant Journal, 1 (2), 4-29

ASM 2011 Conference: New Orleans

2011-05-21T23:12:00.000-04:00

I have arrived in lovely New Orleans! For the next couple of days, I'll be spending my time at the general meeting of the American Society for Microbiology in lovely New Orleans. I'm here at what will likely be my last ASM conference with the Slonczewski Lab from Kenyon College, where we are presenting our recent work on multi-drug efflux pumps, pH homeostasis, and fluorescence microscopy. It's really a great education for the undergraduates that my PI, Dr. Joan Slonczewski, brings along to the meeting.

The opening session was this evening and, I think, much better than the previous two years. Each of the three lectures was intriguing, accessible, and well-prepared. I was reassured that I will be heading off to graduate school in the right direction - evolution and ecology - by the fact that I found the lecture by Dr. Nicole Dubilier on symbiotic relationships between sulfur-oxidizing bacteria and marine invertebrates most enjoyable. Similarly, last year in San Diego at ASM 2010, I thought the best opening lecture was that by Dr. Nancy Moran, who spoke about her work on the relationship between endosymbiotic bacteria and leafhoppers that I wrote about last year.

The second lecture by Dr. Liping Zhao was equally fascinating. He discussed what eating well does for us physically via our microbial gut flora. This work has been in the news somewhat, but I found the thorough lecture perfect for tying together all the disparate pieces of the story. His work shows that for morbidly obese people, a change in diet from a high fat, low fiber diet to a more sensible one allows the microbiome in the gut to shift from an abundance of pathogenic organisms that can cause longterm disease to beneficial and benign organisms. For some reason, the attendees at the reception after the lectures seemed much more restrained around the over-abundance of food in the exhibit hall...

The last lecture, which I found the most difficult to follow from the detail and fast pace, was on environmental stressors that can trigger heritable changes in the organisms studied, mostly yeast. We're not talking Lamarckian giraffe's neck scale of environmentally acquired traits, but the analogy was striking.

That's all for now, but I may check in at least once more during the meeting if I'm not too exhausted in the evenings. Tomorrow we dine at the Court of Two Sisters, which sounds exciting.

Backyard biology: New greenhouse

2011-05-11T23:16:00.000-04:00

Since I've made the decision to accept my admission offer to Ohio State University's Evolution, Ecology and Organismal Biology PhD program beginning in autumn 2011, assuring my presence in central Ohio for several more years, Adam and I decided to take advantage of a great deal on a greenhouse:

Yes, it's a rickety aluminum-frame polycarbonate panel 6' × 8' that probably won't retain very much heat in an Ohio winter, but at least I have something I've always wanted! Adam and I spent last weekend digging out the site, leveling the foundation lumber, and hauling stone to fill in the base. Once the landscaping grows in, we should have a fantastic little hide-away nook behind the greenhouse, perfect for an Adirondack chair or two.

The greenhouse will not be heated much in the winter, making it the perfect spot to overwinter hibernating Sarracenia, like those I just received from the North American Sarracenia Conservancy (NASC).

These Sarracenia alata seedlings are propagated by members of the Grower Committee at NASC from legally-collected parent plants to maintain the genetic variety of these rare and threatened carnivorous plants. The plants I received today were from Texas, Louisiana, and Mississippi. If I do everything right, they'll grow, flower, and possibly be reintroduced in suitable locations. Many of the plants NASC acquires are from boggy habitats that are bulldozed in the name of progress or road widening. This is an excellent example of ex-situ conservation and is meant to be a complementary component to land acquisition and conservation easements (in-situ conservation).

I suppose I'm still thrilled with the idea of having my own greenhouse just steps away, but I imagine I will become less enthusiastic about it this winter when I need to trudge out there through feet of snow.

Is the common teasel carnivorous?

2011-05-09T23:03:00.000-04:00

Dipsacus fullonum, the common teasel. An "urn" type
water storage, where dead arthropods collect.
Source: Björn Appel at Wikimedia Commons.

Dipsacus fullonum, the common teasel or Fuller's teasel, is an asterid native to Europe, Asia, and northern Africa, but is also introduced (and sometimes naturalized) in many other parts of the world, including North America. You would probably recognize it as a common weed with the distinctive comb-like inflorescence. 19th century naturalists recorded finding dead arthropods in the water-collecting cups formed by the fusion of leaves around the stem. Early suspicions for this structure focused on a protective function, since ants are unlikely to cross the water barrier to prey on the flowers.

However, the idea that the plant could be deriving some benefit from the dead insects evolved at least as early as 1877 when Francis Darwin, who, possibly influenced by his father's book, Insectivorous Plants published in 1875, submitted a paper on the topic to be published in the Proceedings of the Royal Society of London. Since then, there have been additional field observations and laboratory experimentation, especially those of Miller Christy in the 1920s, but, as F. E. Lloyd noted in his 1942 tome The Carnivorous Plants, there still was no experimental proof of carnivory. So does the common teasel derive any benefit from the prey it captures in the water urn?

The short answer is yes. Now we have experimental evidence that suggests the plants derive benefit from feeding dead dipteran larvae. Peter J. A. Shaw and Kyle Shackleton of Whitelands College, Roehampton University in London described their results in a recent article published in PLoS ONE. They found that while supplemental feedings of larvae to the plant did not increase overall above-ground biomass, both the seed biomass and seed mass-to-biomass ratio were significantly larger in plants that were fed. The authors note that the results need to be replicated, but this initial finding suggests Dipsacus fullonum meets one of the criteria to be considered a carnivorous (or paracarnivorous) plant.

Bravo to the researchers. It will certainly be interesting to see how the carnivorous plant research and enthusiast community reacts to this news. It's still uncertain how the plant derives the benefit from prey, but it's becoming more clear that Dipsacus fullonum is a candidate for status as a carnivorous plant. What exactly is a carnivorous plant, though? The exact criteria for establishing evolved carnivory and not just a happy paracarnivorous accident has been debated for years and will be the subject of a later post.

Shaw PJ, & Shackleton K (2011). Carnivory in the Teasel Dipsacus fullonum - The Effect of Experimental Feeding on Growth and Seed Set. PloS one, 6 (3) PMID: 21445274

Nepenthes!

2011-04-15T21:48:00.000-04:00

Nepenthes! I've had a proliferation of Nepenthes putting out pitchers, so I went around taking photos today. From the top left across the rows: Nepenthes boschiana × densiflora, N. jamban, N. maxima × trusmadiensis, N. alata, N. ventricosa (? from Lowe's), Nepenthes "Miranda", N. mikei, unknown Nepenthes hybrid that looks like Nepenthes x henryana to me, and N. mikei again.

I've been growing Nepenthes for about 5 years, but until now I have not had any flower for me. And of course, it had to be the one that I rescued from the Lowe's deathcube!

Nepenthes ventricosa with inflorescence from a Lowe's deathcube

Utricularia sucks: Aquatic carnivorous plants that evolved vacuum traps

2011-02-27T23:09:00.000-05:00

"Hi." Trap of Utricularia inflata, clearly showing
the door, trigger hairs, and concave walls.
Scale bar = 500 μm
Source: Vincent et al., 2011.

Utricularia, commonly known as the bladderworts, is a genus of approximately 230 species of carnivorous plants that have evolved an amazing suction trap to supplement their nutrient requirements by trapping and digesting convenient little arthropoid or crustacean packets of nitrogen, phosphorous, and other essential chemicals. Not all species are aquatic, as this cosmopolitan genus has also evolved species with lithophytic (growing in or on rocks), epiphytic, and terrestrial habits.

The rootless aquatic species are most notable for their tiny underwater bladder-shaped traps dotting the web-like system of stolons like aquatic chandeliers. Each trap is only a few millimeters long or less and possess a trap door surrounded by sensitive hairs that trigger the trap door mechanism to open, quickly sweeping the water - and any tasty prey contained therein - adjacent to the trap into the bladder. Keep in mind that each trap is only two cell layers thick when considering the pressure differentials and forces involved in prey capture.

Gazing upon this wondrously evolved botanical curiosity, naturalists in the 19th century thought that it was a passive system as comically illustrated in F. E. Lloyd's 1942 book on carnivorous plants (see below). Charles Darwin and others thought prey was simply enticed into entering the trap, much like a mouse entering a passive mousetrap. Since that time, and thanks to Lloyd's research in the early 20th century, we now know that the bladder traps of Utricularia are much more complex, involving the active setting of a trap and a rapid response once triggered, as illustrated in Lloyd's figure (below), which can only be described as the potential inspiration for the elaborate and beguiling board game Mouse Trap. Rube Goldberg would be proud!

Source: F.E. Lloyd. 1942. The Carnivorous Plants. Waltham, Mass.: Chronica Botanica Co.
The description is too long to reproduce here, but the following amused me: "...which allows the lever l to swing
downwards when the door is actuated again by, it is confidently hoped, a second mouse. In the meantime, the mouse
first caught can employ his time admiring the interior effect, and possibly suggest improvements." (pg. 267)

So by the mid-20th century, we had a pretty good idea of how these traps worked. Water is pumped out of the trap, producing the familiar "set" concave wall appearance. An unlucky crustacean, perhaps a Daphnia, swims too close to the trigger hairs, which relays that signal to the trap door, which swings open so quickly, no one had been able to quantify it before now. And here's where the exciting new research comes in. Physicists decided to record prey capture using high-speed cameras and measure the morphology of the door as it opens. The best thing about this, I believe, is that they put all of their supplemental material on YouTube.

The above video from the new article shows a copepod from the genus Cyclops being trapped by a Utricularia inflata bladder. The whole process occurs in less than one millisecond and is thus one of the fastest plant movements known. The poor little copepod seems utterly stunned. And no wonder! Olivier Vincent at the Laboratoire Interdisciplinaire de Physique, University of Grenoble and colleagues estimated that fluid velocities entering the trap can reach 1.5 meters per second (approximately 3.4 miles per hour) with maximum fluid accelerations of 600g. (Most humans lose consciousness at 4-6g.) Furthermore, in the video above you'll notice the copepod swirls down and around in the trap. The authors propose an interesting idea, that the trap morphology propels prey forward, then down into a swirling motion, preventing the immediate escape before the trap door closes again.

More impressive is the work they did investigating the door morphology as it opens. I can only imagine how precise this microscope, camera, and laser setup had to be in order to capture the exact moment when the door buckles and lets water flow in:

The also produced a dynamic simulation of the door opening:

So there we have it. Amazing new research adds to our understanding of one of the most unique carnivorous plant capture mechanisms. We've come a long way from Darwin's day and I certainly hope there's more to uncover. I'll leave us with just one more video, produced directly by the authors and posted on YouTube:

References:

Vincent O, Weißkopf C, Poppinga S, Masselter T, Speck T, Joyeux M, Quilliet C, & Marmottant P (2011). Ultra-fast underwater suction traps. Proceedings. Biological sciences / The Royal Society PMID: 21325323

IPPP #3: Pinguicula primuliflora

2011-02-23T11:06:00.000-05:00

The third installment of the Infrequent Plant Profile Project, a project I began a while ago at my old livejournal account. I know that I will not stick to a schedule if I designed one, so I choose to make this project informal and infrequent. These will be profiles of plants that interest me and of the circumstances of their original description.


Pinguicula primulaflora "Rose" - the multiple-flowered variety Source: Alexander (fischermans) at the International Carnivorous Plant Society forums.

Today's species is Pinguicula primuliflora C.E.Wood & R.K.Godfrey, the primrose butterwort, is a carnivorous plant from the Southeast United States. As a member of the carnivorous plant genus Pinguicula (family Lentibulariaceae), this species shares the characteristic fleshy, sticky leaves that capture and digest arthropod prey that are unable to escape. This provides the plants with nutrients that are lacking or unavailable from the peaty or sandy soils they inhabit.

A photo of one of my first plants, which
I quickly killed due to my inexperience
growing this genus. I've had much more
success now.

Pinguicula primuliflora was first described by American botanists Carroll Emory Wood and Robert Kenneth Godfrey in a 1957 paper published in Rhodora, the journal of New England Botanical Club. Their work at the time was focused on researching the flora of the southeastern United States. In the course of their work, they made many collections, including other well-known species from the region, including P. caerulea, P. lutea, P. pumila, and P. planifolia. Their specimens revealed a fifth species that had not previously been described. Pinguicula primuliflora is found from southwestern Georgia and western Florida to southern Mississippi. It is distinguished from the other southeastern species by its showy Primula-like flower and its unusual ecology for a Pinguicula, being found in the shade of evergreen shrubs and wherever there is flowing water.

It is surprising that a species could have been overlooked by so many botanists working in the southeastern US until 1957 when P. primuliflora was formally described. This just goes to show how important extensive research into the flora of a region is. It also provides us with an example of how rigorous research, a large sample size, and careful measurements of morphological characteristics of closely-related species can reveal unique populations worthy of recognition at the rank of species or subspecies.

Today, P. primulaflora is one of the most widely-cultivated Pinguicula species and can be found frequently in hardware stores, often in the appropriately-named "Death Cubes." It is a prolific species, producing many rooted clones where leaves touch the soil substrate. Many cultivars of this species exist, including a spectacular double-flowered variety (pictured above)

C.E. Wood Jr., & R.K. Godfrey (1957). Pinguicula (Lentibulariaceae) in the southeastern United States. Rhodora, 59, 217-230

A Genlisean Effort: A Tale of Two Trans-Atlantic Dispersal Events in the Carnivorous Plant Genus Genlisea

2011-01-15T22:58:00.000-05:00

An illustration from 1858 on the closed and open Atlantic Ocean.

South America and Africa look like they fit together snuggly, like puzzle pieces. It's so intuitive that children can grasp this notion without the aid of a formal education in geology. As an accepted theory, plate tectonics draws on evidence from several supporting disciplines, including paleontology and biogeography. Paleontology and geology are, of course, the primary fields where evidence for continental drift arises, the theory being largely proven by work from the recently deceased Dr. Jack Oliver.

Evidence also comes in the form of the remarkably similar flora and fauna and the evolutionary patterns found within certain taxa. However, we must be careful with examinations of extant plant species. Despite the great distance, a remarkable number of plant genera have made the journey and now have established representative species on both sides of the Atlantic. Susanne Renner, of the University of Missouri and Missouri Botanical Garden at the time, published a review in 2004 of the 110 flowering plant genera in 53 families that have dispersed across the Atlantic. She based her work on a 1973 publication by the botanist Robert Thorne (of the Thorne system of classification) and expounded on the likely dispersal routes. Thorne, who lacked key data from gene sequences, identified 111 genera with trans-Atlantic dispersals. With the advantage of 31 years and molecular clock data, Renner revised this number by subtracting genera proven to not be monophyletic and adding previously unrecognized genera. Most of these dispersals appear to be recent in terms of geological time and water currents can carry dispersal in both directions across the Atlantic, while wind currents are typically only responsible for transport from South America to Africa. Renner also thoroughly discounts the common speculation that plant trans-Atlantic plant dispersal could have been aided by birds, noting that it's unlikely given the circumstances of bird migration, dispersal, and digestion (frugivorous birds empty their guts frequently, so it is unlikely any seed eaten would survive the journey).

Genlisea violacea.
Photo source: Noah Elhardt

Renner, writing in 2004, does note that one genus, Genlisea, has a disjunct distribution due to "entry from the boreotropics" instead of long-distance dispersal. In other words, the evidence at the time pointed to a larger northern hemisphere distribution of the genus that crossed the North Atlantic either on then-connected land masses or over short spans of water. She therefore excludes it from her analysis.

Genlisea is an interesting genus of about 22 species found in tropical South and Central America and Africa, including Madagascar. The center of diversity in South America appears to be in Brazil, where up to seven species may be found in one area. The species, commonly called corkscrew plants, are carnivorous, specializing in protozoans and small crustaceans. They're also rootless. The semi-aquatic or terrestrial plants are anchored by their corkscrew-shaped traps that are actually modified subterranean leaves or highly modified stolons. There are some lovely publications out there with nice SEM images of the traps, but most are being paywalls, so you can feast your eyes upon these. Further, the entire Lentibulariaceae family, of which three carnivorous genera (Genlisea, Pinguicula, and Utricularia) seems to be undergoing really rapid evolution to the point that some species, such as Genlisea margaretae, are shedding their genomes. Genlisea margaretae in particular currently holds the title for smallest known angiosperm (flowering plant) genome, with some chromosomes as small as bacterial chromosomes. Researchers believe that this rapid evolution could be the result of significant mutations they found in the key respiratory enzyme cytochrome c oxidase, which could be producing more reactive oxygen species, causing great damage to the plant's DNA, including whole helix-breaks and nucleotide substitutions.

Current distribution of Genlisea; colors indicate number of species in a given area. Figure from:
Fleischmann et al. 2010. Molecular Phylogenetics and Evolution, 56: 768-783.

But beyond their fascinating morphology, carnivorous habits, and genetics, Gelisea are an interesting genus for their trans-Atlantic dispersal, now supported by data published in 2010. The data, consisting of three chloroplast DNA sequences from as many species as they could get their hands on, collected by Andreas Fleischmann and his colleagues indicate that the genus originated in the Neotropics, likely in present-day Brazil. There are two main divisions in the genus, one of which is wholly confined to South America (subgenus Tayloria). The other subgenus (Genlisea) originated in Africa, but one small clade of this subgenus are only found in the Neotropics. The authors first weigh the arguments for an ancient emergence of Lentibulariaceae when South America and Africa were still connected as Gondwana, but this idea is rejected since the family Lentibulariaceae is known to be relatively younger than the Gondwanan breakup. Instead, they propose the remarkable idea that the genus was established in Brazil, dispersed to Africa (likely by fast-moving currents in the Atlantic on "floating mats"), diverged and evolved in Africa, then made a second dispersal back to South America, where a group of species, which have a greater morphological and genetic affinity to those found in Africa, are located. Their case for this theory is well-supported. Just think about how amazing this is, though. Two dispersal events: a colonization of Brazil by subgenus Tayloria, then long-distance dispersal to Africa (founding subgenus Genlisea), a speciation event in Africa, a dispersal back to Brazil and subsequent re-colonization by members of subgenus Genlisea. I don't know about you, but I'm exhausted just thinking about the magnitude of this ~~herculean~~ genlisean effort.

References:
Renner, S. (2004). Plant Dispersal across the Tropical Atlantic by Wind and Sea Currents International Journal of Plant Sciences, 165 (S4) DOI: 10.1086/383334

Fleischmann, A., Schäferhoff, B., Heubl, G., Rivadavia, F., Barthlott, W., & Müller, K. (2010). Phylogenetics and character evolution in the carnivorous plant genus Genlisea A. St.-Hil. (Lentibulariaceae) Molecular Phylogenetics and Evolution, 56 (2), 768-783 DOI: 10.1016/j.ympev.2010.03.009

Honey Run Waterfall

2010-11-17T23:36:00.000-05:00

Topographical map of Ohio with Knox County
outlined. Adapted from the Ohio Department
of Natural Resources (link).

Knox County, Ohio has the advantage of straddling a geological transition zone between the glaciated and unglaciated Allegheny Plateau. The county seat, Mount Vernon, lies in the valley in the western part of the county, on the leading edge of the Wisconsin glacier (the most recent glacial period). The glacier entered the county from the West and pushed toward the East. Of course glaciation ebbs and flows. While Mount Vernon abuts the firm boundary of Wisconsin-glaciated features, the glacier had pushed eastward as to the edge of the county at some points, leaving only the extreme northeast unglaciated. My copy of the 1961 State of Ohio Department of Natural Resources' report on the geology of Knox County (by Samuel I. Root, Joaquin Rodriguez, and Jane L. Forsyth) shows the boundary near Mount Vernon to be a differentiation between the recent Wisconsin glaciation and the distant Illinois glaciation that pushed further East than the Wisconsin.

Of course lower elevation river valleys conduct glacial activity and the prominent Kokosing River flows eastward through the county. East of Mount Vernon is the little unincorporated community of Millwood and the Honey Run Waterfall area, owned by the Knox County Park District. It's a fantastic park with hiking trails and the only waterfall in Knox County. Honey Run empties directly into the Kokosing River in an area with excellent examples of blackhand sandstone, perhaps better known from the Hocking Hills area of Ohio. Surrounding the Honey Run park are ground moraines and terminal moraines of Illinois glaciation derivation. The blackhand sandstone formations in and along the Kokosing River appear to be Wisconsin rock terraces. This unique area in Knox County also provides local nature enthusiasts with a drastically different flora to study. Here we find a disjunct boreal habitat more often found in Canada today. There are large hemlocks that dominate the view of the waterfall, teetering precariously on sandstone cliffs. I always love going to this park for that not-of-this-state feeling with its aberrant geology and flora. It just doesn't feel like Ohio, or at least how I think Ohio should feel - you know, plains full of corn, wheat, and soy. It's true that's how much of Western Ohio appears, but here? Here is a little slice of Canada (or at least its typical boreal habitat) in the middle of Knox County.

And if you've never been to Ohio, I bet you always thought it was completely flat. Surprise!

Honey Run Waterfall in February.

The Kokosing River at Honey Run, looking West. Notice the Blackhand
sandstone on either side of the river. Taken in October.

The sandstone is really easy to write in. Antique graffiti.

Cladonia furcata, I think - a grey reindeer lichen.

8th International Carnivorous Plant Society Conference (1/2)

2010-10-16T17:28:00.000-04:00

Hortus Botanicus, Leiden, the Netherlands

In the beginning of August, I and approximately 120 other participants traveled to Leiden, the Netherlands, for the 8th International Carnivorous Plant Society (ICPS) conference held at the amazing Hortus Botanicus. The conference was hosted by the Dutch carnivorous plant society, Carnivora, and they did a fantastic job organizing the lectures, associated carnivorous plant exhibit, and all the extras. This will serve as my trip report for this meeting.

I arrived jet-lagged on 5 August, flights courtesy of my generous brother-in-law who shared his excess frequent flier miles. (Thanks, Doug!) I hadn't been to Europe in 9 years and I've never been outside the historic splendor of Italy, so this was a real treat to spend a little less than a week really getting to know Leiden. I was immediately awe-struck by the impressive Dutch rail system and how easy, clean, and fast it was. It puts the US Amtrak system to shame (but really, what doesn't?). Leiden is just a single stop from the Amsterdam area airport Schiphol; what a beautiful city! I learned a few lessons while here: Nearly every Leiden resident is willing to help you with directions and are used to it since their city is a confusing network of small alleys interrupted by canals. Nearly every resident speaks excellent English and are more than willing to try it out on a native English speaker. And, at every opportunity, go for a walk. This city is extremely walkable and gorgeous, filled with history and beautiful architecture. This is the city where Rembrandt was born in 1606, where one of Barack Obama's ancestors, Thomas Blossom, lived as an English immigrant on his way to America with a group of Pilgrims (the Dutch are very proud of that connection to Obama and had a very prominent plaque in the square where the Pilgrims once lived), and where Anna Cornelia Carbentus, Vincent van Gogh's mother, is buried. The central city is compact, ringed by a many-pointed star-shaped canal built for defense purposes and dotted with impressive public parks. Who can resist such European charm?

One of the many amazing displays in the
Wintergarden at Hortus Botanicus, part
of the public exhibition complementing
the ICPS conference. Bravo!

Putting my awe aside and getting over the jet-lag-induced migraine, I ambled down the road the next morning, avoiding the plentiful bicycle commuters and entered the gates of the Hortus Botanicus, the oldest botanical garden in the Netherlands. Hortus Botanicus Leiden was first begun as a project for university students of medicine in the late 16th century; the very first prefect of the gardens was the famous Carolus Clusius, whose bust greets you as you enter the gardens. The weather was perfect and mild, especially inviting to someone escaping the heat of the Midwest United States in normally sweltering August. I was awash in a multicultural group, understanding very little (ok, perhaps nothing) of the many languages being spoken over my head. It was awesome and a bit intimidating. After checking in, it was just about time for the first of many lecture sessions.

The first lecture session included a talk by Australia's Allen Lowrie on Australian Drosera (sundews), a discussion by Gert Hoogenstrijd on his trips through Venezuela to the Table Mountains where many rare carnivorous plants are found, a report by François Mey on his incredible efforts to study the Nepenthes flora of Indochina, and lastly a thorough trip-report style lecture by Andreas Fleischmann on the Drosera and Roridula of South Africa. Truly a cosmopolitan collection of speakers and topics! I really do commend the organizers on working very hard to include something for everyone.

Allen's lecture captivated me the most, but the take-home message from all lectures seemed to be that there is so much more work to do in terms of systematic study of species, specimens, and species complexes to tease out the real evolutionary relationships and taxonomies. This was true for Allen's Drosera and Gert's Heliamphora and certainly the Nepenthes of Indochina have their own systematic issues when it comes to the circumscription of species, subspecies, and varieties. Such topics are best left to the experts and it was great to see such expertise on display.

Sarracenia flava var. cuprea in the impressive

Wintergarden canopy walk above the main collection.

The Drosera fascinate me most of all, so I suppose this is why I found Allen's lecture the most compelling. My notes are scattered since he spoke quickly, but there were many gems within his lecture, including the fact that there's an Australian Drosera in the petiolaris complex that survives under water for one and a half months among tadpoles and that there are so many truly distinct species to split from existing species complexes. The breadth of his knowledge on the topic comes from decades of field work that allows him to accurately distinguish minute differences among populations. My notes from Gert's lecture are sparse, but one interesting note is that the South American endemic species Utricularia quelchii is likely pollinated by hummingbirds. A common characteristic all these lectures shared was the splendid and impressive photos displayed during each one. I can hardly imagine what previous generations of botanists did without digital cameras!

I'll stop here and post the remaining trip report, including two more days of lectures, later.

Nepenthes 'Alata'

2010-10-08T20:57:00.000-04:00

It's always interesting to go back through old photos and realize how your plant specimens have grown, given the proper care and treatment. I happened to pick up this Nepenthes 'Alata' from Oakland Nurseries in Delaware, Ohio in August 2007. It had a Deroose Plants tag on it, so it is likely is the Nepenthes 'Alata' cultivar that they produce. I'm not sure of the hybrid parentage, but it obviously has heavy Nepenthes alata influences.

28 August 2007, right after I first got her.

13 August 2008. Almost a year later and she has grown so much! Still in the original pot, but not for long.

3 October 2010. I moved her to the Kenyon College greenhouse and repotted in a much larger container. She has gotten so large now that I tie up the longest lianas on the greenhouse infrastructure. The longest liana measures at over ten feet and she's still growing!

The great golden digger wasp, the Concorde fallacy, and free will

2010-07-24T14:22:00.000-04:00

Sphex ichneumoneus, the great golden digger wasp, about to enter her burrow.

A few weeks ago, I noticed some alarmingly large insects that resembled wasps outside the front entrance of the biology building at Kenyon College. They would fly a few centimeters above the sandy gravel, no doubt surveying the best landing spot. Only a handful of these solitary wasps were here hovering over at least a dozen wasp-diameter holes in the loamy soils under this protected overhang. Suddenly, one landed and disappeared into her burrow. Ah! Digger wasps! I had read about them but never before observed them in the wild. Well, as wild as a well-manicured college campus is in the relative calm of summer. The wasps were a mixture of brilliant orange contrasted with a deep black color. Almost blue iridescent wings fluttered periodically as they danced around the burrows. After consulting available guides and experts in the natural sciences division at Kenyon, it was confirmed these are indeed the great golden digger wasps (Sphex ichneumoneus). These beautiful solitary wasps emerge in the summer and spend about 6 weeks building multiple burrows that they then provision with paralyzed katydids. When the female - the males do not assist in burrow building or provisioning - is satisfied with her stash, she lays a single egg and closes the burrow, commonly completing this process 10 times before her short adult life is over. This species is common to much of the United States, so it's not a surprise to find them here in Ohio.

The sheltered gravel/sand area outside Higley Hall at Kenyon College is the perfect burrow building habitat for the great golden digger wasp.

My usual curiosity of the natural world doesn't typically extend beyond plants, but my interest was piqued. When searching for information on species I have not encountered before, I am often disappointed. Indeed, the great many species out there have been described in full maybe once - the original description - and mentioned a handful of other times in other publications as simply being an associate of other species. It's unusual to find such a detailed account of the life history of a single species, but I was pleasantly surprised with Sphex ichneumoneus. This species and its relatives have been observed in great detail and their behavior has made our species ponder the nature of philosophical fallacies and free will. What a creature!

Investment and return
Over six breeding seasons in the 1970s, H. Jane Brockmann recorded data of wasp behavior from three sites. Typically, each female will work on her own to dig and provision her burrow, but sometimes two females will begin provisioning the same nest in 5-15% of cases. The interloper takes advantage of the other wasp's spent investment and the two will be bringing katydids into the same nest. But because they spend most of their time away from the nest seeking new prey, it is only a coincidence if the two meet and fight over the nest. Fights last between 2 and 16 minutes and often the loser would leave and never return. Because of this one-on-one interaction where both insects have varying degrees of past interest (their future interests would be identical), the data can be thought of in simple game theory mechanics. The founding wasp took the time to dig the burrow and begin provisioning it, while the joiner risked being discovered and the subsequent fight to cheat and not build her own burrow. When faced with a fight, however, each has the same prize and motivation: a well-provisioned nest is worth fighting for, saving the winner days more of additional digging and hunting to lay a single egg.

The "sunk cost fallacy," or Concorde fallacy, so named because the British and ~~American~~ French governments continued to fund the faster trans-Atlantic Concorde flights even when there was no longer any economic incentive to do so, refers to decisions based on past investment because of loss aversion instead of on the rational potential future gains. Brockmann, along with Richard Dawkins, asked the question, "Do digger wasps commit the Concorde fallacy?" in their 1980 publication. The available evidence suggested that the wasp with the least prior investment in a burrow would give up first in a fight and abandon her effort. This result was not skewed by size advantage, which wasp visited the burrow most recently, or whether the winner was the founder or the joiner. Put plainly, the winner was usually the one who brought the most katydids to the burrow. As Brockmann and Dawkins say, "It is hard to resist the suspicion that the wasps are behaving as if following the Concorde fallacy." But are they?

Number of katydids each fight participant brought. Nine fights were over empty burrows. From Dawkins & Brockmann, 1980.

Further, the fight length was strongly dependent on how many katydids the loser brought. Falling into the Concorde fallacy, you might conclude that the loser will fight more vigorously because of greater prior investment in the burrow and less vigorously for those she has barely begun to provision. The losing wasp appears to rationalize: "Fight only as long as is proportional to your individual investment in this burrow." This case study informed the ongoing discussion of whether we humans consider such strategies to be "good" in our assessment relative to their evolutionary stability. The Concordian strategy versus the strict economist (fight based on potential future gain) is fully revealed here in this brilliant case study.

Free will
Just one more quick interesting note about these creatures. In Daniel Dennett's book Elbow Room, he reproduces an account by Woolridge in 1963 about the deterministic behavior of Sphex ichneumoneus. Woolridge watched the wasps return to their burrows with katydids, leaving them just outside while they went inside to inspect. Normally, the wasp is inside for a few seconds, then reemerges and drags the paralyzed katydid backward down into the burrow. He decided to alter the pattern to see if the wasp's behavior changed. When the wasp entered the burrow, Woolridge would subtly move the katydid a few inches from the burrow threshold. The wasp reemerged to find he prey moved, dragged it back to the threshold, then dove back into the burrow alone to inspect again. Woolridge writes, "On one occasion this procedure was repeated forty times, always with the same result." The wasp appears to be an unwilling participant in a free will experiment. She is not a free agent, but instead is driven by environmental cues: once a katydid is near the threshold, I must inspect the burrow and only then can I bring it inside. This property, an apparent lack of free will, was even given the name sphexishness. Dennett notes that publications on free will are rife with fears of sphexishness. Call it genetic determinism or a behavioral loop. Perhaps, though, we're all a little sphexish.

And what of the wasps?
I know their short adult lives will be over soon, but I've enjoyed viewing them through the window these past few weeks. Apparently, though, their lives were meant to be shorter than usual. I walked out the door the other day and noted the acrid smell of pesticides on the air. It got stronger as I approached the burrows and each hole was wet, as if it had been sprayed. Sphex ichneumoneus is a solitary wasp that is not inclined to sting anything but katydids. If you approach them or their burrows, they fly away, bothering no one. I was told our department administrative assistant tried to fill the holes in one day and I suspect she alerted the maintenance department to their presence, thus leading to their demise. Perhaps if people took the time to find out more about the supposed threat before eradicating it, they might change their minds about the course of action. That at least one good motivation for effective science education.

DAWKINS, R., & BROCKMANN, H. (1980). Do digger wasps commit the concorde fallacy? Animal Behaviour, 28 (3), 892-896 DOI: 10.1016/S0003-3472(80)80149-7

Endosymbiotic bacteria in leafhoppers

2010-07-05T17:13:00.000-04:00

Graphocephala coccinea, the candy-striped leafhopper. Source: Wikimedia Commons.

Several weeks ago, urbpan posted about this pleasantly colorful species, Graphocephala coccinea, commonly known as the candy-stripe leafhopper. (cottonmanifesto also took some amazing photos of this species and displays one here.) If you live in North or Central America, you would probably recognize this species as a common visitor of gardens and cultivated areas. Urbpan noted that leafhoppers are frequently vectors of plant diseases including many bacterial infections that are often species-specific.

Less frequently realized is a bacterial relationship of another kind: symbiosis. Perhaps by now, more than 40 years after Lynn Margulis' stunning work popularizing it, the endosymbiotic theory of the origins of many organelles within the eukaryotic cell, including mitochondria and chloroplasts, is widely understood enough to continue without comment. But briefly, there is a heap of undeniable evidence that many of the eukaryote's organelles were once free-living bacteria that were engulfed and put to work by other cells: mitochondria respire, chloroplasts photosynthesize. It is reasonable to assume other such relationships exist within certain lineages of eukaryotes.

So here we have leafhoppers, like many other insects including aphids, feed almost exclusively on the phloem or xylem fluid of plants. With such a restricted diet, you are bound to run into nutritional deficiencies. Syrup is tasty, but I wouldn't want to subsist solely on it! What's an insect to do? The clear answer is to harvest those little nutrient-producing biological machines known as bacteria.

An electronmicrograph of the bacteriome of Homalodisca coagulata. The plentiful irregular spheroids (E) are the bacterial symbionts, Baumannia cicadellinicola, the border at the top (B) is the bacteriocyte (single cell) boundary, and the large organelle in the middle (N) is the host cell nucleus. The scale bar is 10 μm. The cell is just packed with bacteria, isn't it? Source: Moran et al. 2003.

The plant fluids usually consist of carbon and nitrogen sources such as amino acids, the building blocks of proteins. Xylem fluid chiefly contains non-essential amino acids such as glutamine and asparagine. Whereas most animals are incapable of modifying those raw materials into every other essential amino acid, vitamin, or cofactor they need thus requiring them to supplement their diet with foods with high concentrations of these necessary items, sap-sucking insects have solved the problem by entrusting the production of these necessary chemicals to their bacterial symbionts. These obligate intracellular bacteria are held within special organs called bacteriomes. The symbiotic bacteria are heritable, often transmitted from mother to egg, leading to interesting evolutionary questions. Some insects even have multiple symbionts which provide different chemicals for the host. For example, the glassy-winged sharpshooter (Homalodisca vitripennis) possesses a Gammaproteobacteria that provides vitamins and cofactors, while the Bacteroidetes (a different phylum entirely from the other symbiont species) synthesizes many of the essential amino acids.

Even more astonishing is the rate of genome size reduction seen in these symbionts. As is the case with the mitochondrion found in humans that harbor only 37 functional genes, the genomes of sap-sucking insect bacterial symbionts is heavily reduced. In the above glassy-winged sharpshooter example, the two bacterial symbionts have complementary genomes; that is, each genome has lost the functional genes that the other is responsible for.

Phylogenetic analysis of the hosts and symbionts reveal common evolutionary relationships, meaning that the relationships among the insect species is highly correlated with the symbiotic bacteria found within them. This indicates that the original infection and symbiosis was an ancient event occurring millions of years ago. Molecular clock data suggests that the common ancestor of the symbionts found in two genera in the subfamily Cicadellinae, Graphocephala and Homalodisca, lived sometime between 80 and 175 million years ago, which correlates well with the data on the divergence of the host insect species.

So next time you see these little garden pests think of all the complex reactions and relationships between host and symbiont when that leafhopper is feeding on your plants and admire the interesting evolutionary history of these organisms before you flick it off your prize raspberry bush.

References:

Moran, N., Dale, C., Dunbar, H., Smith, W., & Ochman, H. (2003). Intracellular symbionts of sharpshooters (Insecta: Hemiptera: Cicadellinae) form a distinct clade with a small genome Environmental Microbiology, 5 (2), 116-126 DOI: 10.1046/j.1462-2920.2003.00391.x

Wu D, Daugherty SC, Van Aken SE, Pai GH, Watkins KL, Khouri H, Tallon LJ, Zaborsky JM, Dunbar HE, Tran PL, Moran NA, & Eisen JA (2006). Metabolic complementarity and genomics of the dual bacterial symbiosis of sharpshooters. PLoS biology, 4 (6) PMID: 16729848