Sandy plants: a paper, an update, some wacky plant photos.

A little while back, I published a paper that Rick and I had been working on for awhile. In short, there are quite a number of plants which entrap substrate – sand, dirt, etc. – on their surfaces with sticky trichomes. These species occur worldwide in dunes, beaches and deserts. Quite a number of people, dating back to the late 1800’s, had hypothesized that this “sand armor” must protect the plant, but nobody had actually gone out and tested it. So we tested both the hypothesis that it is physically defensive (who wants to chew on sand?) and that it is a form of camouflage (since of course, it makes the plant look like the background).

Abronia pogonantha, one of the sandiest plants I’ve seen. Photo: EL.

We found support for the physical defense hypothesis (in two tests) and did not find any evidence that the camouflage protects the plant. You can read (Inkfish – one of the best science blogs) or hear (Quirks and Quarks) more about this project.

The best part of publishing this was hearing from a prominent researcher (who had noticed this phenomenon), that he tells his students: “if you don’t believe that sand is defensive for the plant – try sandpaper instead of toilet paper!” Since publishing this, I’ve been able to continue this research and observe quite a few more cool sandy plants – some of which were new to me and some of which I had only heard of.

The best sandy plant in the world. The common names for Pholisma arenarium include “scaly-stemmed sand plant”, which is my personal favorite plant name ever. About an inch tall. Near Morro Bay, CA. Photo: EL

In that paper, there is a list of sand-entrapping plants. Many of these I had seen and noticed. Others were from published literature. I surveyed a bunch of really good naturalists and they suggested many others (their list was the longest). That is how I happened upon Pholisma, pictured above. This odd plant is a borage (the family includes some wellish-known plants including borage, heliotrope, fiddleneck, baby blue eyes, phacelia, etc.). Looking like a lump – maybe a mushroom? – it is completely chlorophyll-free, instead sucking nutrients from nearby plants (it is an obligate parasite, like Indian pipe, Monotropa, in the east). And the coolest part, of course, is how much sand it catches – it is nearly completely covered! It is very possible that plants which coat themselves in sand suffer a photosynthetic cost because less light reaches them. For Pholisma, that doesn’t matter at all!

LOOK AT ALL THAT SAND! (I am pretty sure those purple things are flower buds – I didn’t unfortunately get to see a flowering individual).

Pholisma was, since I learned about it last year, the top of my list of must-see plants and seeing it was one of my spring highlights so far. I happened upon it accidentally while looking at another sand-entrapping plant, Abronia umbellata (I used Abronia latifolia in my experiments).

Abronia umbellata is not as sandy as some congeners, but it is pinker than most! (there is also a really, really, cool paper on floral evolution in this species – check it out). Photo: EL.

The central coast of California has three species of Abronia which grow in close proximity on coastal dunes. Abronia maritima is generally on the beach while latifolia and umbellata are a little farther up (and occasionally grow over each other). They each catch sand to some extent.

Abronia maritima. The yellow anthers are positioned right above the stigma and seem to drop pollen onto it (from my couple flower dissections). It has far smaller flowers than the other species. I’d bet quite a bit that it is selfing. Photo: EL.
Abronia latifolia, the common sand verbena for most of the California coast. Common doesn’t mean boring though, its quite awesome. Photo: EL
My labmate/collaborator, Patrick, found this bizarre plant. My best guess – and it was pre-fruiting, so I can’t be sure – is that its an umbella x latifolia hybrid. It had leaves reminiscent of latifolia (large, broad, very fleshy but held upright like umbellata and somewhat in between the two in glandularity) and stems which were stickier than umbellata, but very red like umbellata. The flowers were too long for an abberant maritima (and leaf structure wrong), but seemed fine for either latifolia or umbellata (though with aberrant coloration). Jury is out. Thoughts? Photo: EL

Abronia are awesome (everyone knows that already) but there are some smaller, more inconspicuous plants that are also really good at sand-catching.

This is Tiquilia plicata. It mostly grows as a little roadside weed in the Mojave. It catches lots of sand on the margins of its leaves (!) and stems. Margins of leaves are usually where caterpillars and other chewing insects begin feeding… (hand-wavy adaptationist explanation over). Like Pholisma, it is also in the borage family. Photo: EL


Tiquilia has nice flowers, but you have to look really hard to find them (they are tiny). This was a tall individual growing in a less-sandy spot (hence the lack of sand on the leaves and stems in the photo – the bottom still had lots). Photo: EL.
Another new favorite plant was Centrostegia thurberi. A tiny, cherry red, spiny bizarre thing, it is mildly sticky and has bracts encircling its stems which catch lots of sand – seemingly with stickiness and also just being shaped like a bowl. This was another favorite.

Centrostegia thurberi. Photo: EL.


It catches a lot of sand on its stems, but… (photo: EL)


It also does this! Dipsacus – teasel – often has these sorts of bracts that fill with water and mosquito larvae and stuff. I’ve never seen bracts full of sand before (and every plant had them!). Photo: EL.

And lest I turn completely into a botanist, there were some insects, too. Importantly, there was one caterpillar – Hyles lineata – that was really common in a bunch of spots on Abronia. This species, the white-lined sphinx moth, is common over much of North America some years and absent others. Fortunately for me and unfortunately for many herbaceous plants, it is having a good year in southern California (especially near Anza Borrego).

This Abronia villosa is not as happy as I am about this big (3″+) final-instar caterpillar. Photo: EL.

While Hyles likes to eat Abronia (I’ve found them on pogonantha, latifolia, umbellata and villosa this year), they not like to eat sand at all. While it doesn’t have a good mechanism for taking it off, it seems to concentrate on nonsandy plants first and then on nonsandy parts of the plant, but it always ends up eating the sandy parts of the plant eventually.

A green-morph H. lineata on pogonantha. They come in lots of colors – black, green, yellow and all manner of in-betweens. They all seem to turn into identical moths. Photo: EL

Unsurprisingly as they don’t like it, sand on plants is damaging to them. A normal Hyles mandible at pupation looks like this:

An SEM micrograph of the right mandible of a Hyles lineata fed on nonsandy Abronia latifolia. Those “teeth” are for grinding up the plant before it enters the body. Photo: EL

But if they eat sandy plants, they get pretty rough:

Look at the “teeth” – or lack thereof – on this right mandible, from a caterpillar feeding on sandy A. latifolia. Photo: EL

That’s it for today: a description of a study, some weird sandy plants, and a teaser of a future paper…

Data I’ll never publish: Antirrhinum herbivory

Inspired by this post, I’m going to try to put the results of small (but interesting) experiments up here every once and awhile. In the summer of 2014, I spent a lot of time washing plants. I was – and still am – curious of the function(s) of plant exudates. I primarily did this with Trichostema laxum and Atriplex rosea (in 2013), but I also did it with Mimulus layneae and Antirrhinum cornutum (California snapdragon). The snapdragon gave me interesting results.

(this post should also be regarded as potential project for someone else: I started it in May – there is plenty of time to get up to McLaughlin and do it again this year).

One of the experimental A. cornutum, showing leaf damage.

This snapdragon, while not as heavily glandular as Trichostema or that Mimulus, is fairly glandular-sticky, even entrapping a small number of minute insects (see the table/supplementary material). Under the microscope, you can see the fairly dense short glandular trichomes (the longer trichomes are mostly nonglandular) on the stalk and flower bud.

Stem of A cornutum with an entrapped insect.
Flower bud showing short glandular and long nonglandular trichomes.

Wondering whether the glandular exudate is defensive, I did an experiment where I removed it with water. Most glandular exudates in CA summer annuals seem water soluble, so a spray bottle rainfall takes off much of the exudate (observationally verified in situ with a 20x loupe – plus whatever was in this exudate made suds on the plant!). This manipulation was my first treatment group. Of course, adding water to a plant has an effect of its own, so I also had a water control group, where I added the same amount of water below the plant’s leaves, as to not wash off any exudates. Finally, I had a true control group, which received no water whatsoever. I instituted these treatments on the 30th of May and reapplied them on the 17th of June. Each time, I recorded the number of leaves, flowers, fruit, and plant height, as well as any damage. I also checked the plants, but did not reapply treatments on the 2nd and 19th of July (the last check all were senescent).

During the experiment, plants suffered two main forms of herbivory. The first type, which was most common and most destructive, was that the stems were entirely clipped off. I’m nearly positive this was by jackrabbits (indicated by a single flat cut diagonally across the stem) and it usually killed the plant. The photos below shows what remained.

A killed experimental A. cornutum plant. See it?!? Its the little stem to the bottom left of the flag. Also notice a nice healthy Lessingia in the background. They, too, are extremely glandular and sticky.
A survivor of mammalian herbivory. If the meristem was not completely destroyed, they often came back and branched like this. Like the classic overcompensation “herbivore-plant mutualisms”, the resulting plants were often bigger than the others, with more reproductive structures, but unlike this “mutualism”, it was too late in the season and they had low fitness, as they could not mature these structures.

The mammalian herbivory was not random. Of the 25 plants per treatment, 11 in the control group, 13 in the rainfall simulation (exudate removal) and a whopping 20 in the water control group were eaten by mammals (this is nonlethal, lethally was 10, 12, 18). With a simple chi-squared test, we can demonstrate that this was likely nonrandom (X2 = 7.3688, df =2, p = 0.025) (for lethal, X2 = 5.5714, df=2, p = 0.062). Why were the mammals targetting the water control plants so heavily?

Were they bigger and thus easier to find or just more profitable to eat? They were not significantly different in height, fruit or flower numbers from the other two groups during any check. I don’t have data on plant quality (perhaps the less water-limited plants were more nutritious or something?).

The other type of damage was equally-interesting. Heliothis phloxiphaga is a generalist caterpillar on glandular plants. It was the primary herbivore on my columbines, as well as a common herbivore on Trichostema laxum and other sticky plants. Like most heliothiine noctuids, it feeds primarily (but not exclusively) on reproductive structures. I only observed it once on Antirrhinum (eating a fruit), but all the fruit damage I found was consistent with it (and that’s one more time than I saw a jackrabbit eat it!).

The other type of damage: caterpillar fruit predation.

I had hypothesized, that if the exudate were defensive, the washed plants would be most heavily eaten. This hypothesis was supported with the fruit damage. Rainfall plants received far more damage than the other groups. (note: I didn’t actually analyze this with zero-inflated binomial, as it should be. There is a problem, in that only 7/25 of the water control plants had any fruit at all because of the rabbits.)

A crumby excel graph of proportion fruits damaged.

What does this all mean? Obviously, it means that mammalian and insect herbivores are responding to different plant traits. What they are exactly, I’m not sure (especially for mammals). If anyone (nudge, nudge, wink, wink) were to repeat this experiment, with a larger sample size, and maybe some other mechanistic experiments (perhaps cage controls and lots more trait data to see what is different in the water control and rainfall manip groups), I think its a pretty good system that someone could get a paper – if not a few – out of.

New paper: plant external chemical defenses!

When I came to grad school, I was convinced I’d be working on plant-caterpillar-parasitoid relationships, with a focus on plant chemistry or biocontrol. I wrote my NSF-GRFP on the artichoke plume moth and several of its parasitoids. I spent a few months looking for plume moth caterpillars on thistles (a scratchy job) with relatively little success, though not for lack of trying. My focus then shifted to a cute little butterfly, Brephidium exilis, with strange population dynamics and then parasitoid sex ratios. All of these failed (either through logistical problems or me half-assing them because they just weren’t that interesting to me).

And then I happened onto Blitum (=Chenopodium) californicum at Bodega and my research took an unexpected turn. As I describe here, I was fascinated by the little fluid-filled pockets on leaf surfaces. I ran a number of small tests and found a defensive function of the bladders (probably one of many, many functions) and wrote it up and it was quickly published in Oecologia, a good journal. This being the very beginning of my second year of grad school (fall 2013), I was pretty jazzed. My committee, however, thought that I should be working on “the bigger picture”. And so the ideas for this new paper on external plant defenses came about.

Writing this paper was WAY harder than I thought it was going to be. Instead of a formulaic paper, here’s why I did the study (intro), here’s how I did it (m&m’s), here’s what I found (results) and here’s why its important (discussion), I was faced with a blank slate. I could write this however I wanted and that was a bit daunting. Primary and secondary school taught me how to write a coherent 3-5 paragraph essay, secondary school and college taught me how to write a term paper and college and grad school have taught me how to write a scientific paper, but no one taught me how to write a synthesis/idea/review paper. I’m glad I did it, though I think it will be a few years before I start on another paper like this.

This caterpillar (an unidentified pterophorid) lives on a plant (Hemizonia congesta) with lots of glandular trichomes, the factories of many external defensive chemicals. It blends in nicely with its “glandular trichomes”. 

Taking Rick’s lab motto, a Buckminster Fuller quote – “dare to be naive” – to heart, I started by thinking of what ecological differences would occur if a defensive plant chemical was situated on the plant surface instead of inside plant tissues. I came up with five basic differences between chemicals on the surface of plants (external chemical defenses: ECDs) and those inside plant tissues (internal chemical defenses: ICDs):

(1) they are in direct contact with the abiotic environment;
(2) they are not in direct contact with plant tissues apart from the cuticle;
(3) they are first contacted by the vast majority of interacting organisms;
(4) they may contact more than just the feeding and digestive parts of interacting organisms;
(5) they are secreted from specialized structures or cells (or derived from a secretion thereof).

As discussed in a prior post, glandular exudates are often sticky and can have cool tritrophic effects. Here is a mayfly (Ephemeroptera) stuck on serpentine columbine (Aquilegia eximia). 

I then took this list and delved into the literature, reading hundreds of papers on plant chemical defenses over a several month period (I cited 180 in the final paper, but probably skimmed or read abstracts of  twice that number). While external chemical defenses had not been formalized as a class, many wonderful studies had investigated plants with ECDs and I was able to find many examples both in terrestrial systems and in marine alga. I wrote up a massive tome – over 18,000 words – with carefully detailed natural history of many of the studied systems. Of course, this was not publishable, though I was proud of it (I like nothing more than to put cool natural history into an ecology/evolution framework). I worked and worked on cutting it down to its basics. In the process, I found more references and presented it at ESA last year, getting some more feedback. The process dragged on and I got more and more interested in doing experiments and less and less interested in this mammoth synthesis paper. I submitted it a couple times in various stages of cutting and was basically told it was too long. So after this past field season, I sat down for a couple weeks with no other distractions and made it into a far more focused paper, which I submitted to Biological Reviews, as it was still a bit long for most other journals. Fortunately, it was accepted with helpful reviews and after tossing a few minor points back and forth with the editor, it is now out for you to read!

Without getting into the specifics (you can read them in the paper, if you so choose), I found that many chemicals are on plant surfaces, many of these chemicals are defensive, and these may be systematically different from internal chemical defenses in the ways I hypothesized. This paper is important for three reasons: 1) hundreds of papers are published on plant chemistry and plant chemical ecology each year, but it is ecologically important where certain chemicals are located; 2) we have a rich body of theory on plant chemical defenses, but some parts of it are rather untested, and ECDs may allow some tests of certain theories (e.g. optimal defense theory) and; 3) many important crop plants have external defenses, which are easily manipulable in many cases, and it may be useful to think about them in this way to come up with better pest management schemes.

I’m really curious about how this paper and this new classification scheme is received. Am I just cluttering the literature with new terms, or are these ecological differences informative and useful? We will see!

Castilleja minor, a species of paintbrush and a hemiparasite, has really cool oily exudates. The pictured caterpillar, possibly an Autographa (?) species, seems undeterred, though it does mostly eat the insides of the flowers and fruit, which may avoid the exudates.