Wednesday, August 3, 2016

Answer: Mind the gap!

Things are often not what they seem...  

Recall this week's Challenge:  We're trying to understand what's causing this gap around the plants up in the chaparral on Black Mountain (in the Santa Cruz range).  

1.  What causes the odd, plant-free gap around the plants in these photos?  

What struck me about each of these pictures is that there's a noticable gap between the green plant and the grassland next to it.  Oddly, this doesn't happen ALL the time, but it does happen a lot.  

The plants here are chamise (Adenostoma fasciculatum), but I'm pretty sure I saw gaps like this around coyote brush (Baccharis pilularis) in the same area.  

What's going on here? 

I began my search with: 

     [ plant free zone OR area near chamise OR "coyote brush" ] 

but these results weren't especially good.  I learned a lot about how to create "plant free zones" around houses, especially those that are built in chaparral or near fire-prone plants like chamise.  I also learned a great deal about chamise, such as: 
"Under natural conditions, dormant seeds accumulate in the soil until stimulated by fire to germinate [66,126].  Chamise seeds are unpalatable and seedbanks apparently are not subject to heavy predation [111]. Consequently, chamise seed densities increase over time [133].  Seed density in the seedbank beneath 9-year-old stands was estimated at 2,000 seeds per square meter while in 85-year-old stands, seed density was approximately 21,000 seeds per square meter [132]."  (From the Federal Fire Effects Information system, which includes descriptions of plants like chamise.)

Reading through these articles was interesting, but not especially useful.  (Or so I thought.  See below...)  

I modified my query to focus in on just chamise: 

     [ plants not grow near chamise ] 

and I had a bunch of new, additional results about chamise.  But one result struck my eye, a PDF from the Santa Cruz County Parks Department that said (in the snippet) "...chamise uses allelopathy, altering the soil as it drops leaves..."  This sounded as though it MIGHT be relevant, so I clicked through to the landing page and found these lines that sounds like our solution... 
"Some plants engage in chemical warfare, or allelopathy. Chamise accumulates toxic, water-soluble compounds as a result of normal metabolic processes. Fog drip and rain carry these toxins to the soil, where they inhibit the growth of competing plants."
Now this sounds like the right mechanism--this very well might cause a zone around the chamise that would be pretty barren.  However, this paragraph uses a word that's new to me: "allelopathy," so...   

I looked it up: "allelopathy" means"the chemical inhibition of one plant (or other organism) by another, due to the release into the environment of substances acting as germination or growth inhibitors."   This very well could be exactly what's happening to cause the plant free zone around the bushes.  Broccoli and black walnut, for instance, both exude substances that kill (or prevent from growing) plants living nearby.  So, maybe we've found the answer.

And now that I know this word, I remembered seeing it before--in the first set of results!  Now I know what that word means, and I see in retrospect that my first hint was actually in the first search I did, if only I'd known.

This is now officially interesting, so I dug a little deeper into the "allelopathy" vein.  

I thought what I'd do is to search for "allelopathy" for chamise, with the obvious query:   

     [ allelopathy chamise 

Not only did I find a lot of new results, but I found myself in the middle of a scientific battle of explanations!! 

Look at the results page here: 

As I read the first result, I was astonished:  this link gives you an idea about what's going on.  In that article, published in 2004 (in the oldest botanical publication in the US) the author calls into question the idea that chamise is allelopathic.  So I did a bit of searching and reading of these pages.  Here's what I found:  

On the "allelopathy side" are publications that argue that chamise IS allelopathic, and causes the plant-free zone around chamise: 

Keeley, J. E., Morton, B. A., Pedrosa, A., & Trotter, P. (1985). "Role of allelopathy, heat and charred wood in the germination of chaparral herbs and suffrutescents"  The Journal of Ecology, 445-458. 
McPherson, J. K., & Muller, C. H. (1969). "Allelopathic effects of Adenostoma fasciculatum, "chamise", in the California chaparral"  Ecological Monographs, 39(2), 177-198. 
Muller, C. H. 1953. "The association of desert annuals with shrubs" Am. J. Botany 40: 53-60. 
Muller, Cornelius H., Hanawalt, R. B., McPherson, J. K. "Allelopathic Control of Herb Growth in the Fire Cycle of California Chaparral" Bulletin of the Torrey Botanical Club 95(3)  (May - Jun., 1968),  225-231 

Notice that these publications are all a few years old.  Science marches on.  We should look for more recent work.  

There are a few more recent publications that argue this is all wrong, that allelopathy isn't really what's going on here (at least for chamise):
Halsey, Richard W. "In search of allelopathy: an eco-historical view of the investigation of chemical inhibition in California coastal sage scrub and chamise chaparral." Journal of the Torrey Botanical Society (2004): 343-367.   
Weidenhamer, Jeffrey D. "Distinguishing resource competition and chemical interference: overcoming the methodological impasse." Agronomy Journal 88.6 (1996): 866-875.
After reading a bunch of these papers, it becomes clear that the idea that chamise is allelopathic originated in Muller's original paper from 1953.  But that since then, the idea that chamise actively emits chemicals (or, more likely, that the chemicals are leached off in rainwater over the plant) has been called into question.  

There's no doubt that some plants do emit compounds that suppress nearby growth, the question being debated here is whether or not chamise is one of them or not.  The articles are fairly detailed, with long sections describing how to test one idea or the other. Fascinating reading, if you're into details of methodology (which I actually quite enjoyed, but maybe that's just me), but I'll just summarize it by saying these folks are still trying to figure it out.  However... 

A very nice summary of this entire debate is contained in a relatively recent book, Perspectives on plant competition (2012) by James Grace and David Tilman.  They conclude that allelopathy by chamise and other chaparral plants is "...overrated... if not altogether fictitious..." (p 146).  

Why this might matter is because some botanists are trying to figure out ways to harness plants natural allelopathic capability to do weed suppression in fields, and perhaps farm without using any weedkiller sprays on the crops.  In essence, if chamise IS allelopathic, might it be possible to breed (or genetically engineer) a food plant that needs no weedkiller, but can grow just fine on its own?  

HOWEVER.. while reading Perspectives on plant competition, I looked up each of the citations of Muller's work, and in particular each reference in the text about allelopathy.  In the process, I found this remarkable phrase on page 145.  

"... experimental evidence supporting an alternative explanation for the bare zones around chaparral shrubs.  Batholomew (1970) demonstrated that halos around some shrubs in the soft chaparral might be maintained by herbivory from animals inhabiting the shrubs. Successive attempts to test the relative importance of allelopathy versus herbivory in both the development and the maintenance of bare zones showed that chemical inhibition occurred in some species, but not in others and that the herbivory of unexclosed seedlings could be an intense as 100% (Halligan, 1973, 1975, 1976; Christiensen and Muller, 1975)." 
I know that's dense prose, but WOW!  If you decode this text, they're saying that animals are eating the small plants around the shrubs.  (That's what "herbivory" means--animals eating plants.  "Unexclosed" means there's no animal-excluding fence around the small plants just outside of the shrub.)  And not just some of the plants, but up to 100% of them!  

Looking up the Bartholmew reference (Bartholomew, B (1970), "Bare zone between California shrub and grassland communities: the role of animals"  Science 170, 1210-1212), we find that 

"...Previous studies have emphasized the role of volatile inhibitors of plant growth in producing this bare zone. However, there is a concentration of feeding activity by rodents, rabbits, and birds in this zone; if this activity is prevented by means of wire-mesh exclosures, annuals grow in the bare zone. Thus, animal activity is sufficient to produce the bare zone."  

Among other things, we now have a technical term for this region around the outside of chamise and coyote brush:  bare zone.  My next query was: 

     [ "bare zone" chaparral shrub ] 

and--voila!-- we have a lot of articles on the bare zone around chaparral plants, just as we're seeing in the photos.  The consensus of opinion now seems to be that the bare zone is caused by animals that are foraging near the clusters of chaparral shrubs. (Bartholomew, 1970; Halligan, 1974; Bradford 1976Barbour et al., 2000, etc)  

In this long list of articles, there's a wonderful (and very readable) one from Bay Nature magazine entitled "A Landscape Shaped by Fear on Mount Diablo."  In it, the author writes: 

Muller’s work was later challenged by researchers who argued that his work glossed over the role of hungry seed and plant eaters. “In California, the chaparral and coastal sage shrubs form excellent cover for rodents, rabbits, and birds,” Stanford graduate student Bruce Bartholomew wrote in a seminal 1970 paper. 
These small animals leave the shelter of chaparral in search of food. But they don’t go far, lest they themselves become a meal for hawks, bobcats, mountain lions, coyotes and other predators. That’s why the bare zone is also called the “scurry zone.” 
Where Bartholomew set up cages excluding small animals, the bare zone largely disappeared. That and followup experiments led to the view held by many field biologists today, that wary little animals play a huge role in keeping chaparral-grassland borders free of vegetation. In their view, the bare zone is not so much a strip of dirt poisoned by plant chemicals, it’s a landscape shaped by fear.

The article is well worth a read.  In it, you meet UC Berkeley botanist Lindsey Hendricks-Franco and a great picture of the exclosures she's set up to test her hypothesis about small animal herbivory at the margins of burned zones in the chaparral causes bare zones there.  

Of course, not being satisfied with what I'd read, I decided to go back out to my local chaparral and do a few of my own observations.  Here are two photos that are pretty suggestive of what's going on:  

A bare zone beside coyote bush (which nobody believes has any allelopathic effects on nearby plants). 
 Above you see a bare zone next to a large stand of coyote bush.  So far as I know, there hasn't been any report of allelopathy for coyote bush.  If that's true, what's causing the bare zone next to it?  Probably the small animals that live within.  Meanwhile, just down the trail I saw this:  

Grass growing immediately next to a small patch of chamise.

And here you see a bunch of grass growing right next to a small patch of chamise.  If it was truly allelopathic, why would the grass be growing there?  

Note that the stand of chamise is pretty small.  I noticed that small patches of chamise  OR coyote bush don't have bare zones, while large patches of chamise OR coyote brush do have bare zones.  

I speculate that a smallish-stand-alone chamise bush just can't provide the cover that large patches can.  That's why small bushes don't have a bare zone--if you're a mouse, there's no protection.  But a big stand of any kind of chaparral brush will do:  chamise, coyote bush, or even manzanita (another common California chaparral bush).  

The Google Earth photo (from March, 2013) shows this gap effect quite clarly.  Each of these clumps of bushes (some are chamise, some are coyote brush) has a small zone around each that clearly shows the effect of either the allopathic effects of chamise, or the herb grazing effects of small mammals near the bushes.  (Note also the change in the color of the soil near the bottom of the image; it really does change to a very light color down there.  I checked it out in person--this isn't an artifact, it's really a color shift.)    

And, if you look at many of the clumps of bushes, you can see a pretty clear effect of the presence (or absence) of a bare zone depending on the size of the clump of bushes. 

Bare zones seem to vary by bush clump size (and not by what kind of bush it is). These clumps are all taken from the area just to the north of the satellite photo shown above.  The 3 on the right, being fairly small, show no bare zone.

Once the clump gets below a certain size, the bare zone seems to disappear.  (Note that I haven't field-checked this, but I'll run up there this week and measure some of the bare zone widths to see if this really holds. More data when I have some to report.)  

Search Lessons

What I found so interesting about the comment thread this week is that Regular Researcher Remmij first found one explanation for the gap ("Shrub cover subsequently increases numbers of rabbits and small mammals (and birds too) that reduce herbaceous vegetation and favor shrub development [25,54]. Thus, well-established coyotebrush stands generally have depauperate understories [30].")   

Remmij's quotation is from Point Reyes National Seashore and North District of Golden Gate National Recreation Area (N.R.A.), Fire Management Plan: Environmental Impact Statement (2004), and leads directly to the "animals in the bush are causing the bare zone" interpretation.  

But then everyone seized on the allelopathic effect for chamise, probably because that's the first explanation that pops to the front when you do the obvious search.   But note that this is true only for chamise, and doesn't hold for coyote brush and other plants in the area.  

I suspect that what ALSO happened is a kind of piling-on: we all saw the first explanation (allelopathy) and thought "that must be it."  

If that's what happened (and I'm curious about your thoughts, Regular SearchResearchers), then this is an example of confirmation bias at work.  That is, the tendency (when doing research) to latch onto a plausible explanation and then search for reinforcing evidence.  

1. Be careful about confirmation bias!  In particular... 

2. Look for another explanation, or at least another point of view.  In this case, it turned out that allelopathy IS a real thing, but it's probably not what's going on here.  I found the "animals cause the bare zone" story because I noticed that these articles were all a few years old.  So I looked around a bit more and found... 

3.  It's a good idea to find a recent reference to see if current belief is the same as older beliefs.  And in this case, they weren't.  Botanical thinking had changed since the first allelopathic explanations were written.  

Sorry this took so long to publish, but I was busy reading and having a great time looking for examples of this effect.  

Hope you had as good a time as I did with this Challenge.  

This week's Challenge will come out tomorrow (Thursday).  

Search on!  


  1. Good Morning, Dr. Russell.

    Yes, the answer is a surprise!

    Allelopathy was new for me and I tried some queries but never found the key words "bare zone" so yes, I accepted as true the first plausible answer. Even when I read that Chamise was not in the list of plants with allelopathy.

    Thanks for sharing the answer and the links. As always fun with knowledge.

    See you tomorrow!

  2. Confirmation Bias: Did everyone look at the first answer and pile on ? I never look at other replies until after I have submitted my comments, or, if I am totally baffled and have spent way too much time on it, then I look, but do not submit.

    Others ? No idea, but not this kid.


    jon, nifty ideas you have come up with. I saw jackrabbits are there but the 'damage' did not seem like rabbit.

  3. Many years ago, I thought I was being knowledgeable and thrifty when I gathered several bags of eucalyptus leaves to naturally fertilize and enrich the soil in a backyard patio planter.
    Thrifty, yes. Wise, it turned out, not so much.

    1. And now you know why.... Did the soil ever recover?

  4. Replies
    1. I like that hypothesis (coyote brush as snack magnet). I don't think the etymology is clear, but that's a great suggestion!

  5. I'm sorry if I sound like I'm trying to "rain on your parade", and although I admittedly didn't read EVERY line of your post, the high school Biology class that I took many decades ago gave me an answer to your "Challenge" that is conceptually simpler, more obvious, & more parsimonious than what you came up with. Simply, In arid environments, it is large plants whose roots can travel some distance below the surface that can access water in some form that cannot exist in the arid conditions on the surface. The brown/burnt, much smaller plants existing between the larger ones have very shallow roots that can't access the deeper sources of water, and are only really alive during the brief rainy season. As far as why a distance exists between these large plants, that is no more surprising to me than the distance that exists between oak trees in an oak forest. Although an oak tree drops its acorns such that only tiny distances exist between the acorns on the ground, only the "strongest" acorns, and the "strongest" saplings therefrom reach maturity, while the rest perish. ... Joe Kulik ...