Posted by: Jeremy Fox | June 17, 2011

Zombie ideas in ecology

Ideas, once they take root, are hard to kill. Thomas Henry Huxley famously referred to “the slaying of a beautiful hypothesis by an ugly fact” as “[t]he great tragedy of Science”. But like Hamlet, it’s a fictional tragedy—it doesn’t actually happen that way. Ideas, especially if they are widely believed, are intuitively appealing, and lack equally-intuitive replacements, tend to persist. And they persist not just in spite of a single inconvenient fact, but in spite of repeated theoretical refutations and whole piles of contrary facts. They are not truly alive—because they are not true—but neither are they dead. They are undead. They are zombie ideas.

Economist John Quiggin coined the phrase “zombie ideas“, but it isn’t just in economics where undead ideas walk among us. Ecology (and probably every field) has its own zombie ideas. In some cases they’ve survived decades of attacks from the theoretical and experimental equivalents of chainsaws and shotguns, only to return to feed on the brains of new generations of students. But this is 2011, and we have new weapons to deploy against the zombies. Weapons like blogging. Weapons whose effects can spread around the world via the internet like the bullets from a modern-day shotgun, hitting the zombies wherever they are found. Weapons I plan to use, starting right now.

The first ecological zombie in my sights: the intermediate disturbance hypothesis (IDH).

Broadly speaking, the IDH is the idea that intermediate frequencies and/or intensities of ‘disturbance’ or ‘environmental change’ maintain diversity by preventing competitive exclusion. The IDH was coined by Connell (1978) and given influential treatment by Huston (1979) and Grime (1979), among many others, but the idea goes back at least to Hutchinson (1941, 1961). The idea is now in ecology textbooks, such as the one I learned from, Begon, Harper & Townsend (2nd ed.). And refutations of the IDH have been around for a while, too. Mackey and Currie (2001) gave an empirical refutation, reviewing over 100 experimental tests of the effect of disturbance on diversity and finding that the predicted peak of diversity at intermediate disturbance levels hardly ever occurs (<20% of experiments). But more important are theoretical refutations, since a logically-invalid hypothesis literally can’t be supported (or rejected) by empirical evidence. Chesson and Huntly’s (1997) attack on the logic of the IDH and related ideas is one of my favorite papers of all time. Roxburgh et al. (2004) and Shea et al. (2004) are very good too, although they pitch their refutation as a ‘clarification’ of the IDH, a rhetorical strategy which certainly has its virtues but which also has the unfortunate drawback of letting readers think that there’s some kernel of truth in the core ideas which spawned the IDH. There’s not. In my view, zombies are beyond redemption, and trying to see the good in them while closing our eyes to the bad only exposes more people to the bad. Students especially often find it difficult to distinguish good ideas from superficially-similar bad ideas. Rude as it may sound, the only thing to do with zombie ideas is to kill them off, without mercy.

Here are the three zombie ideas at the core of the IDH:

1. Disturbance reduces species’ densities, thereby weakening or eliminating competition and preventing the competitive exclusion that occurs in undisturbed environments. But too much disturbance kills off all but the most disturbance-tolerant or quickest-recovering species, hence intermediate levels of disturbance support the highest diversity.

This is a seductively appealing idea (so maybe a better analogy than zombies would be the alien seductress in the movie Species). And it’s totally wrong. Yes, disturbances reduce species’ densities and thereby weaken competition. But as Chesson and Huntly (1997) point out, they also reduce the strength of competition needed for exclusion! Seriously, I cannot believe this zombie is so hard to kill. Anything that reduces your per-capita growth rate (disturbance, continuous sources of mortality, environmental ‘harshness’, etc.) also reduces the amount of growth that competition (or any other factor!) needs to subtract in order to push you into negative territory. Or, if you prefer to think in terms of abundances rather than growth rates (you shouldn’t, but in case you do), anything that reduces your abundance also reduces the number of individuals that competition (or any other factor) needs to subtract off in order to reduce your abundance to zero.

And if you’re the sort of person who only believes data, not math, well, I’m sorry for you, but fortunately for you the very nice paper by Violle et al. (2010) experimentally confirms theoretical refutations of this zombie idea.

2. Disturbances interrupt competitive exclusion by temporarily reducing all species to low density and weakening competition, thereby allowing all species to subsequently increase.

This is Huston’s (1979) version of the IDH, which he supported with some simulations of a Lotka-Volterra competition model with periodic, density-independent mortality events. Which just goes to show that mathematical models are ineffective weapons against zombies if you don’t fully understand your models. To his credit, Huston (1979) didn’t claim that disturbances in his model produces stable coexistence, but he did claim that they slow competitive exclusion. Which, again, is a really seductive idea (I’m starting to think I should have called these ‘alien seductress’ ideas…). I mean, you take a competition model which exhibits rapid competitive exclusion, you add disturbance, and you get much slower exclusion. Which means that disturbance slows exclusion, right? And if you look at the simulated time series, you see that all the competitors increase after each disturbance. Which means that disturbance slows competitive exclusion by interrupting it, right?

Wrong. Adding disturbances (here, density-independent mortality events) to a disturbance free model changes two features of the model, not one. Obviously, it prevents the model from reaching a deterministic equilibrium. But (apparently) less obviously, it changes the long-term average mortality rate. The correct ‘control treatment’ for Huston’s (1979) numerical ‘experiment’ is not his disturbance-free model. It’s a model with continuous mortality at the same long term-average rate as in the model with disturbance. And if you simulate the correctly-controlled experiment, you find that the fluctuations in Huston’s (1979) model are irrelevant to slowing competitive exclusion. What slows competitive exclusion is the increase in the long-term average mortality rate, which reduces the growth rates of all species, and so reduces the difference in growth rate between competitively superior and inferior species, thereby slowing the rate of exclusion. In Chesson’s (2000) terms, increased long-term average mortality rate in this model is an equalizing mechanism, but not a stabilizing mechanism. And fluctuations in mortality in this model are no mechanism at all—the visually-obvious short-term fluctuations they create in species’ abundances have precisely zero effect on the long-term outcome.

Our first two zombies illustrate a source of zombie strength which we’ll encounter again in a moment: failure to appreciate that long-term average dynamics are ultimately what matters. Disturbances matter if, and only if, they alter long-term average dynamics. They’re just noise otherwise. As Hutchinson (1961) wrote, “Mere failure to obtain equilibrium owing to external variation in the environment does not mean that the kinds of competition described mathematically in the theory of competitive exclusion are not occurring continuously in nature.”

Unfortunately, having fought off the two zombies discussed above, Hutchinson (1961) immediately (in the very next paragraph!) fell victim to a zombie idea of his own:

3. If, due to fluctuating environmental conditions, the identity of the dominant competitor changes on an intermediate timescale, no one species will ever have time to exclude the others and all will coexist. Overly-slow fluctuations will allow exclusion to take place before conditions change. Species will average across overly-fast fluctuations, and whichever species competes best on average under the full range of environmental conditions will exclude the others.

This is Hutchinson’s (1961) own favored solution to the ‘paradox of the plankton’, the apparent coexistence of dozens of species of planktonic algae in apparently-homogeneous lakes in which only a few resources and other factors could ever possibly be limiting.

When I teach my undergraduate ecology students about the consequences of environmental fluctuations, I start by showing them this zombie idea, and I read them some statements of it from Hutchinson (1961), and from ecology textbooks, just to make sure they’ve got it. And then once I’m sure they understand it and have got it down in their notes, I throw the textbooks against a wall and yell, “Now cross that out because it’s wrong!” I’m not kidding, I really do this. My hope is that by parading a zombie in front of them, and then executing it in dramatic fashion, I’ll immunize them against any future attacks.

Varying the relative timescales of environmental fluctuation and competitive exclusion is not sufficient, on its own, to affect long-term average competitive outcomes. Here’s the right way to think about it. Imagine a constant environment, in which species A is favored over species B (i.e. has a higher per-capita growth rate). Species A of course will exclude B in the long run. Now imagine that the environment fluctuates, but that it mostly favors species A; it only favors species B quite rarely (say, 1% of the time). Now, without worrying about the frequency with which the environment changes and assuming all else is equal, tell me: which species do you think will win? If you’re like the undergrads I teach, you immediately said “Species A—it’ll just take a little longer”, which is absolutely right (well done!) Now imagine that the environment favors species A 51% of the time, and species B 49% of the time. Which species do you think will win? That’s right, species A still wins, it just takes a really long time. Finally, imagine that the environment favors each species exactly 50% of the time. Which species wins? The answer, of course, is neither, at least in a deterministic world (if there’s demographic stochasticity, one species or the other will eventually drift to extinction, just as with neutral genetic drift in evolutionary biology). Notice that we never said one word about the timescale on which the environment fluctuates. Because all that matters is which species is favored on average. Indeed, constant conditions that slightly favor species A would lead to exactly the same long-term outcome as fluctuating conditions that favor species A slightly more often than species B.

I think part of the reason ecologists succumb to Hutchinson’s zombie idea is that they focus on the opportunities created by fluctuating conditions. Competition is wiping some species out, we think, so we need some mechanism that gives those species an opportunity to grow. And yes, fluctuating conditions that temporarily favor one species over another do create an opportunity for that favored species to grow. But when conditions change, that creates an opportunity for a different species—which means a lack of opportunity (or better, the opposite of an opportunity) for the previously-favored species. You can’t have your cake and eat it too. You have to take the bad with the good. What fluctuating conditions giveth, fluctuating conditions taketh away.

So much for our third zombie. Let me put down my shotgun and talk about the implications of this battle.

It’s important to recognize that the above refutations are not empirical; they’re logical. The zombie ideas refuted above literally cannot be correct. If you argue that “All men are mortal, and Socrates is a man, therefore Socrates likes ice cream,” your argument is incorrect (more precisely, ‘invalid’), and no amount of data showing how much Socrates likes ice cream can make your argument correct. Analogously, there certainly are environments in which competition is weak. But the consequences of this are not correctly described by the zombie ideas discussed above. And there certainly are systems where diversity peaks at intermediate disturbance. But the reasons for this are those discussed by Chesson and Huntly (1997), Pacala and Rees (1998), Roxburgh et al. (2004), Shea et al. (2004), and Miller et al. (2011), not the zombie ideas discussed above.

Broadly speaking, disturbances and fluctuating conditions matter because, and only because, of nonlinearities and nonadditivity. In a linear, additive world, all that matters is long-term average conditions, because the effects of good times and bad times cancel out in the long run. But in a nonlinear, nonadditive world, the effects of good times and bad times no longer cancel out in the long run. For instance, temporal fluctuations in the identity of the dominant competitor can promote coexistence—if species have some way to take full advantage of the good times and then ‘store up’ those advantages while somehow avoiding or minimizing the damage of the bad times. That idea is what Peter Chesson calls the ‘storage effect’; it turns out that ‘storage’ is a form of nonadditivity.

I’ll conclude with a few zombie-fighting lessons, distilled from the above, which you can use to protect yourself not just against the IDH zombies, but against any other zombies which might try to eat your brain (I’ll be slaying some of them in future posts).

1. Don’t trust your intuitions without doing the math. Your intuitions about ecology, unaided by mathematics, are mostly worthless. Don’t feel insulted; mine are too. So are everyone’s. Ecological systems are complex, dynamic, and characterized by feedbacks rather than ‘one-way’ causality; verbal intuitions about such systems are notoriously unreliable. The people who originally developed the IDH are some of the smartest and (deservedly) most influential ecologists of all time; this post is not a criticism of them personally. The IDH is not a dumb idea. If it was, it never would’ve ended up in all the textbooks. But just because it wasn’t dumb doesn’t mean it’s not totally wrong. Mathematics (by which I don’t mean primarily mean numerical simulations, I mean analytical techniques like algebra) is a tool which makes us smarter. It forces us to precisely and explicitly define all our assumptions, and to logically work out all their consequences. Words are ambiguous, and logical reasoning of any complexity is immensely difficult. If your verbal hypothesis really is logically valid, you should be able to express it in mathematical form. Probably, you’ll discover that your idea doesn’t work precisely the way you thought it did, or at all. Which means that the math has shaken up your intuitions, and hopefully helped to replace them with better intuitions. And no amount of data is a substitute for doing the math, because data doesn’t interpret itself, you interpret it. Connell (1978) took his inspiration for the IDH from his tremendous empirical knowledge of tropical forests and coral reefs—and it didn’t protect him from the zombies.

2. Just because a famous ecologist, or lots of ecologists, or a textbook, says something doesn’t make it true. The IDH probably would never have achieved the penetrance it has if it hadn’t been developed by some of the most famous ecologists of the last 70 years. That led some ecologists to try to test the IDH. After all, if the G. E. Hutchinson or the Joe Connell proposes a hypothesis, the rest of us sit up and take notice. That led other ecologists to attempt further tests; once a topic becomes ‘hot’ lots of people pile in just because it’s ‘hot’. And once that body of work reached a critical mass, it had to go into the textbooks, which are written and updated to reflect the current state of the field. None of which changes the fact that the IDH doesn’t stand up to logical scrutiny. Remember my earlier post on the importance of contrarian ecology? Well, the penetrance of the IDH is what happens when too few contrarians arrive too late to save us from the zombies.

3. You have to be careful about how you teach ‘classic’ ideas. I teach Hutchinson (1961) because, in order for students to appreciate what’s right about modern ideas like the storage effect, they have to appreciate what’s wrong with classic ideas like Hutchinson’s. I do not teach Hutchinson (1961) as an idea that was ‘further developed’ or ‘clarified’ by subsequent workers, because that just encourages students to gloss over challenging, non-intuitive ‘details’ like nonlinearities and nonadditivities and just focus on seductively simple, apparently easy-to-understand claims. Frankly, I’d prefer not to teach Hutchinson (1961) and other ‘classic’ IDH ideas at all, but because these zombie ideas still walk among us, I’m worried my students will be viewed by others as ignorant if they haven’t at least heard of these ideas.

p.s. Interestingly, evolutionary biologists never fell for the IDH, at least not nearly to the same extent ecologists did. Their textbooks, such as Graham Bell’s Selection: The Mechanism of Evolution, contrast ‘opportunities in space’ with ‘obligations in time’. The idea is that spatial variation in relative fitness (equivalent to what ecologists would call spatial variation in the relative competitive abilities of different species) is a powerful force for maintaining genetic diversity. That’s because each genotype can just live in those locations where it’s fittest and never need experience locations where it’s relatively unfit. But on its own, temporal variation in relative fitness can’t maintain genetic diversity, because different genotypes have no choice but to experience the bad times (the times when they are relatively unfit) as well as the good times. It’s not as if you can use a time machine to avoid experiencing conditions that don’t suit you. In a temporally varying environment, the winning genotype is the one with the highest geometric mean fitness in the long run (which by the way is mathematically equivalent to having the highest arithmetic mean relative fitness (Grafen 1999); natural selection doesn’t work any differently in a temporally-varying environment than in an unchanging one). And although evolutionary biologists tend not to use the same jargon as ecologists, they’re well aware of the nonlinearities and nonadditivities that you have to combine with temporal fluctuations in relative fitness in order for such fluctuations to stably maintain genetic diversity.

I suspect the reason evolutionary biologists never fell for the IDH is that the first evolutionary biologists to consider the effects of temporal fluctuations in relative fitness, and of temporal fluctuations in population size, were mathematical theoreticians like Sewell Wright (1948). Because evolutionary biologists started out with the right, mathematically-derived answer, they were vaccinated against the verbal zombie ideas that later took root in ecology.

It’s interesting that evolutionary papers like Wright (1948) predate Hutchinson (1961). I assume Hutchinson, and the other IDH advocates who followed him, were unaware of Wright’s work, or else didn’t realize that it pre-refuted them. I’d suggest that this is an argument for the virtue of reading widely—except that I wouldn’t want evolutionary biologists to start reading zombie ecological ideas! Just as with variable environments, the variability of what you read doesn’t matter unless you have some way to store up the effects of the good material while minimizing the damage of the bad material.

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Responses

  1. “When I teach my undergraduate ecology students about the consequences of environmental fluctuations, I start by showing them this zombie idea, and I read them some statements of it from Hutchinson (1961), and from ecology textbooks, just to make sure they’ve got it. And then once I’m sure they understand it and have got it down in their notes, I throw the textbooks against a wall and yell, “Now cross that out because it’s wrong!” I’m not kidding, I really do this. My hope is that by parading a zombie in front of them, and then executing it in dramatic fashion, I’ll immunize them against any future attacks.”

    Then you are a very poor teacher, because you don’t read, absorb or understand the literature on the psychology of education. Telling someone a falsehood and then correcting it simply cements the falsehood in their mind. This has been proven repeatedly. So often, in fact, that your own rhetorical style is basically an alien seductress of its own, one to whom you are madly making love.

    • Thank you for the feedback Ben. It would be helpful to me if you could provide a few links to the research to which you are referring. It is true that I don’t read the educational psychology literature, although I have discussed it here and there with my spouse who is a schoolteacher with a psychology degree and a master’s degree in education. Based on my admittedly-limited and indirect understanding of the literature, I suspect that your blanket claim about the undesirability of teaching and then correcting falsehoods comes with caveats and exceptions. For instance relating to the age and educational attainment of the students (I’m teaching college juniors and seniors; I wouldn’t teach this way with, say, elementary students).

      More broadly, while I freely grant that knowledge of educational psychology is valuable to a teacher, so are a lot of other things (and I recognize that you didn’t deny this). I’ve had many excellent teachers who had never read this literature, and so I question whether reading this literature is essential to teaching well, as you seem to believe. For instance, modeling oneself after good teachers, and taking mentoring from them, as I have tried to do, is another approach. I absolutely would not claim I’m the world’s greatest teacher, but on the evidence available to me I am not “very poor”, and I would appreciate if you would refrain from blanket judgments of me as a teacher based on one anecdote I related in one blog post. I receive very good marks on the evaluation forms which students at my university are required to complete, and on exams my students do well on questions which test their understanding of both correct and incorrect ideas about how disturbance affects coexistence. If I had evidence that students were failing to grasp what I was trying to teach them about the IDH, I would teach it differently.

      Nevertheless, I would welcome alternative suggestions on how to approach the subject. As I noted in the post, ‘classical’ ideas about the IDH are incorrect, but well-established in the literature and in textbooks. For that reason, I don’t feel I can simply ignore them in favor of the correct ideas of Chesson and others, although I’m open to argument on this. But if I teach those ‘classical’ ideas at all, then I’m teaching falsehoods, no matter whether I use a dramatic rhetorical style or not. The dramatic rhetorical style of this lecture isn’t so that I can show off. It’s the only lecture of mine in which I adopt this style; it’s not a style which has “seduced” me. The dramatic rhetorical style of this lecture is a conscious strategy to try to get around the very problem you’ve identified: teaching a falsehood risks simply cementing the falsehood in the students’ minds. I’m not wedded to it, and would welcome suggestions on alternative strategies.

      • Ok, I was brief and not entirely constructive. I wouldn’t entirely recommend reading the primary literature in psychology about correcting misinformation. It is as dense as the ecology literature. Loftus 1979 is seminal. “Updating accounts following a correction of misinformation” by Johnson and Seifert, 1998 is just one example of the dense technical literature. “The continued influence of misinformation in memory: What makes a correction effective?” Seifert 2002 is more applied in nature. Nyhan from Michigan makes it very political in a way I don’t really appreciate. O’brien et al 2010 (J. Exp. Psych.) provide an interesting case of correcting the literature about correcting literature.
        In any case, as a teacher, I agree that drama is helpful for holding attention. I also believe many other things about how much material can be presented in a single lecture, etc, that doesn’t seem to make it into common practice. I find it frustrating, hence the outburst.
        I would highly recommend that every college faculty take some teaching classes. The Bok Center at Harvard and the McDougal Graduate Teaching Center are excellent resources. I have taken some methods courses and I continue to read that literature sporadically. A recent book that turns out to be more interesting than expected was Lemov’s “Teach like a Champion.” It can be applied to medical students and graduate students, though it is targetted at K-12 teachers. Another field that is interesting is the parenting literature (like Kazdin), because it draws from the science of reinforcement and learning.

        Essential? Perhaps not, but I think the other comments here on your post reinforce my message that presenting wrong information first – particularly forcefully – is likely to lead many astray. I would recommend, actually, presenting the correct theory first and then walking through the narrative of its development. This way the Zombie doesn’t get in first; and you can be as dramatic as you like.

      • latecomer posts ftw.

        Gilbert et. al. You Can’t Not Believe Everything You Read (http://www.wjh.harvard.edu/~dtg/Gilbert%20et%20al%20%28EVERYTHING%20YOU%20READ%29.pdf)

        Gilbert et. al. Unbelieving the Unbelievable: Some Problems in the Rejection of False Information (http://www.wjh.harvard.edu/~dtg/Gilbert%20et%20al%20%28UNBELIEVING%29.pdf)

        http://lesswrong.com/lw/k4/do_we_believe_everything_were_told/ summarizes some results.

  2. Damn! Then I’m a poor teacher too. Like Jeremy, I have tried to inoculate students against wrong ideas (in economics) using almost exactly the same technique. And yes, with many students, it fails. I have even tried making beeping noises at 5 second intervals when I’m (knowingly) talking total rubbish.

    So, how the hell else do I explain why (e.g.) demand curves in macro don’t slope down for the same reasons as demand curves in micro? When the students, having just finished a whole term in micro, are going to be really tempted to think a macro demand curve is just a micro demand curve writ large?

    • Thanks for the support, Nick.

      By the way, conversation with my wife, who’s an expert in this area, reveals that the use of ‘dramatic’ techniques is apparently a hot idea in educational psychology, and my textbook tossing qualifies as ‘dramatic’ in this sense. The basic idea is that the teacher is creating a memorable moment–no student of mine will soon forget that the IDH is wrong (unless I start tossing textbooks every day or something, and so become the lecturer who cried wolf). Probably the same is true for your beeping noises (I’ll have to try that one…)

  3. The very first class I taught as a new faculty member was a grad seminar on coexistence in a fluctuating environment. We read Hutchinson, we read Chesson and Huntley, etc. And at one point we were discussing Chesson’s ideas and one of my students said something like, “OK, I guess, but I think I’d rather stick with Hutchinson. It’s simpler.” “But it’s wrong!” It was a very humbling moment. My student (students?) had completely missed the point of the last several weeks.

    • Hi Robin,

      Maybe if you make yourself up as a zombie while teaching Hutchinson, that will help. 😉

      Seriously, the first person to figure out a surefire way to get students to give up comforting or ‘easy’ falsehoods in favor of hard or ‘difficult’ truths will deserve the first and last Nobel Prize for Education. But sadly, much as there’s no Philosopher’s Stone, such a surefire technique probably doesn’t exist.

      Depending on the nature of the misconception the student has, it may be possible to undermine it, thereby ‘creating a space’ in the student’s mind which can be filled with the correct way of looking at things. The philosopher Ludwig Wittgenstein once spent a year as an elementary school teacher in Austria. A student came to him one day with a drawing of a circle, representing the earth, with two stick figures standing on it, an Austrian on ‘top’ and a Chinaman ‘underneath’. The student asked Wittgenstein why the Chinaman didn’t fall off the earth. Now, you could try to teach the student that that’s not the way gravity works, that everybody ‘falls’ towards the center of the earth. But I think Wittgenstein’s answer was more effective in terms of undermining the student’s false idea, thereby ‘clearing the decks’ in preparation for learning the truth. Wittgenstein simply took the drawing, flipped it over, and said “Now we fall off.” I wish I could think of a way to ‘flip the drawing over’ when it comes to the IDH.

      BTW, this is emblematic of much of Wittgenstein’s whole approach to philosophy, which he said consisted of “showing the fly the way out of the fly bottle.”

  4. I am a Zombie.
    Not like Bill Murray who merely dressed like one and got shot in the stomach, but more like a proper connoisseur of human brains. I was never very good with mathematics and my only reference to Wittgenstein is the ‘Philosophers Song’ by a bunch of crazy (but lovely) Brits dressed up like Aussies. Like some of the students mentioned in the text I’m not always convinced by simplified theoretical examples. As nature is generally quite obstinate and often refuses to follow the set parameters of theoretical models, I have a hard time accepting them as absolute truth of natural processes. In the example where a fluctuating environment favours species A slightly more often (51%) than species B, A will ultimately win. I keep finding it more likely that both will eventually be eaten (or trampled, overgrown etc) by species C, which was not in the model, and theory can keep predicting their competitive outcomes while they’re both being digested. Throwing books around does not help.

    I’m also not entirely convinced that putting numbers on everything is the ultimate solution to ecological questions. In the same sense that Socrates does not necessarily like ice-cream because he’s a man, you could accurately model or calculate the amount of ice-cream he would eat without answering the question whether he is a man or not. As for the IDH, it still seems to me that everybody agrees (even this blog) that disturbance can maintain and/or increase diversity, the arguments are all about how and why. This is why the hypothesis / model refuses to die. Also, that Mackey and Currie found that it worked about 20% of time for a range of systems, a range of different methods, a range of different ‘disturbances’ and even different response variables, is actually not that shabby.

    I’ve done some manipulative field experiments where disturbance prevented competitive exclusion to occur and made the limiting resource space available in which ‘new’ species settled and diversity increased. The same thing happened the following year in another experiment. This makes me doubt the argument of disturbance being “noise” and irrelevant because long time-scales should be considered (“short-term fluctuations […] have precisely zero effect on the long-term outcome”). What if the time-scale is not infinite? What if the species that shape patterns of local diversity actually do compete over one season, and this struggle starts anew each spring (in the shallow benthic communities that I study) when they come back from wherever they’ve been hiding (does someone know where they go? Africa? Do they bring back coconuts [carried in pairs with a piece of string] like swallows?).

    The theoretical and practical (for lack of a better word) criticism of the IDH seem very similar to me. The 5-7 suggested prerequisites of the IDH on trade-offs, amounts of available species, succession etc are not so far from the arguments of “spatio-temporal niches” and non-linearity. When I observed that undisturbed assemblages was completely covered by tunicates (i.e. 100%), and intermediate assemblages harboured many species, I find it really hard to think that this was not related to preventing competitive exclusion while allowing colonization. You can throw a book at me if you like, or you could call it creation of spatio-temporal niches (which would not be incorrect) and perhaps the growth and competition was not linear and they probably did some storaging while they were at it. But in the end, I’d still say competitive exclusion was prevented, and new species settled in the freed space.

    Sincerely,
    Robin Svensson

    P.S. Very nice blog, just found it yesterday through a friend. That I don’t necessarily agree doesn’t mean that I don’t appreciate it. Also I wish you could publish it as an article like it stands, copy-paste all, including the pics, it’d be a lot more fun to read than the conventional masses of text we read and write =)

    • Dear Robin,

      Thank you for your comments, glad you like the blog even if you don’t always agree with it.

      I entirely agree with you that capturing nature in all its wonderful complexity in a mathematical model is impossible. Nor would we want to. There’s a wonderful Stanislaw Lem story (really, just a fragment of a story) about a map as big as the world itself. Such a map is analogous to a model which captures the entire world in all its detail. It’s obvious that such a map would not only be impossible to create (as you’ve noted), but useless. One’s goal with a model is always to capture some key feature of the world in order to improve our understanding, on the assumption that leaving out some other bits does not inhibit our understanding of how this key bit works, at least not too much. I think a similar assumption is at play when we conduct field experiments, manipulating only a few factors at a time, and measuring only a few response variables, out of all the many factors which surely matter, and out of all the response variables we could’ve chosen to measure. If the world is so complex, and complex in such a way, that it’s impossible to build up an understanding in this way, then I confess I am not sure how else to build up an understanding of it. As I’ve noted in other posts, I highly recommend Bill Wimsatt’s “False models as means to truer theories” for more on the many uses of admittedly false models, and how they help us learn about the world not despite their falsity, but actually because of it. Wimsatt also notes that some ways in which a model can be false are *not* useful; I’ve argued in this post that classical ideas about how the IDH works are false in unhelpful, misleading ways.

      Not sure I quite follow your remarks about my Socrates-and-ice-cream analogy. My point was merely that a logically-invalid model (i.e. a model in which the assumptions do not in fact imply the predictions) cannot be even an approximately true description of the world (this is an example of unhelpful falsity in a model, as opposed to helpful falsity). I certainly agree that the fact that diversity sometimes peaks at intermediate diversity is why the IDH in its classical form refuses to die. As you say, the question is *how and why* diversity sometimes peaks at intermediate disturbance. Where I would gently disagree with you, I think, is in your implication that this occasional predictive ‘success’ counts in favor of the classical IDH. In my view, it does not, because other models, which *are* logically valid, also make the same prediction. In cases where it appears to be right, the IDH is just getting lucky–it’s giving the right prediction for the wrong reasons, which isn’t very hard to do. In general, qualitative patterns like “variable A first increases, then decreases, with increasing values of variable B” are not difficult to predict–many, many quite different models will typically be able to generate such simple patterns. In order to learn where the pattern really comes from, we have to do other things, such as test predictions about other variables, or test how well the model assumptions are satisfied, etc. This is what the Violle et al. experiment, cited in the post, does.

      Disturbance is only irrelevant ‘noise’ on long timescales in a linear, additive world (looking back, I think the post could’ve been a bit clearer on this point). The real world is of course nonlinear and nonadditive (this is one respect in which nature is wonderfully complex). That’s the point of the models of Chesson and others–to show how, in a nonlinear, nonadditive world, the effects of good times and bad times don’t just cancel out in the long run, leaving the long-term average dynamics unchanged. That’s why these models, but not classical models, are able to explain why intermediate levels of disturbance really do sometimes prevent competitive exclusion in the long run. You’re someone who is sensitive to all the details of nature that our models often leave out or oversimplify. Chesson and his colleagues share your sensitivity–which is why their modeling ‘adds back in’ nonlinearities and nonadditivities that classical models omit. I gently disagree that classical models and modern ones really aren’t so different. For instance, classical models and contemporary ones make different predictions about the outcome of the experiment of Violle et al., or about other experiments one could conduct. I think perhaps they appear similar because similar words often are used to describe their behavior. This just goes to show that words are imprecise and often overbroad (see, e.g., my previous post on whether some general ecological ideas are TOO general), and I definitely think theoreticians often are quite poor at explaining their models to others. But then again, inventing different terms every time an existing term didn’t precisely fit our needs would leave the field awash in far more jargon than it’s already awash in…

      I’m flattered that you’d like to see this post in print. The editor of the Oikos “Forum” section is considering whether to publish the occasional blog post as an article, after peer review. But unfortunately or otherwise, I doubt any future publication of this post will include the linked pics. 😉

      • Dear Jeremy, thank you for the response,

        What I meant with the suggested prerequisites being similar to the creation of spatio-temporal niches as an alternative hypothesis to the IDH is that the assumptions are similar. I think this is perhaps also the core of the Zombie when I think about it? The suggested prerequisites for the IDH are roughly a set of condition to be met (diverse system, disturbance releases limiting resource as well as kills or displaces, lots of propagules, competitive exclusion can occur, regional diversity larger then local, trade-offs between competition, colonization and disturbance) in order to observe the predicted pattern. Now, if all conditions / suggested prerequisites are met, I don’t see how disturbance can do anything but create a hump-shaped response in diversity (which perhaps makes it more logic to see how often the conditions are met in nature instead of actually testing the model). But these are not included, and perhaps should not be (?), in the refutation of the IDH. Zombie #1 is (or was) probably alive in my head because I always considered it to be dependent on colonization as disturbance in the definition of Sousa (1984) creates opportunity for establishment by releasing limiting resources. Which makes all the difference, at least to me, when it comes to the possibility of disturbance to increase diversity. And this brings me straight to the article you mention by Violle et al. 2010. Disturbance can never increase diversity if no new species establish in the disturbed environment, without this it only becomes a monotonically decreasing response in diversity. This has been argued by many authors and already in 77 by Osman (in fact prior to the proposing of the IDH if you consider Connells paper), and by articles/books by Sousa, Huxham, Collins and probably others as well. As colonization was not possible in the closed systems in Violles experiment, I don’t see how they could accurately test the models at all. Hence, to me Violle didn’t prove the models wrong despite the high competition at high disturbance, because there was never any way for diversity to increase in the first place. And perhaps this is it? To me the IDH, DEM are dependent on the prerequisites suggested by other authors, and I have considered all this together as the collective work on ecological disturbance, and I never really saw the need to scrutinize the -79 paper by Huston alone, because it was just one of many pieces in the puzzle.

        I guess what I’m asking first of all, is if the IDH (or hump-shaped response based on ideas of the IDH) is complete rubbish also when considering the suggested prerequisites as I have. If it isn’t, should people that improve models rename them or something to show that it’s more than was written when it was proposed? Also, is the model by Kondoh (2001) as inaccurate as the one by Huston (1979)?

        I’ve actually been struggling with these exact questions when writing up my papers and thesis, although most papers are already published now so there may be some undead brain tissue in there. But this is also why I found your post on the IDH as a Zombie very interesting and relevant. It’s a pity with the pictures though, I think you should try and fit them in a future publication! =D

      • Hi Robin,

        It appears you may not be as much of a zombie as you suggested in your previous comment. 😉 What you’re getting at is the fact that the IDH isn’t really any one well-defined hypothesis, it’s a complex of interrelated ideas which are difficult to tease apart in order to sort the wheat from the chaff. You’re certainly right about that. Walking through this entire literature and organizing it is much more than I could try to do in a blog comment. The recent work from Roxburgh, Shea, and colleagues (linked to in the post) might help clarify matters, as they’re very much out to pull together various threads and integrate them into a single unified mathematical model.

        Afraid I don’t quite understand why you don’t see the relevance of Violle et al. Even if there are colonists from outside the system, it’s still the case that any factor (like disturbance) that reduces per-capita growth rates also reduces the strength of competition required to produce exclusion. In general, I don’t think it’s the case, either in classical theory or in more recent work, that colonists from outside the system are essential for the IDH to work. Some models of the IDH, particularly in the context of thinking about secondary succession and successional niches, do include a source of colonists from “elsewhere”. But many models in this complex of ideas, including many that are logically-valid and that predict peak diversity at intermediate disturbance, lack any external source of colonists. I suspect this just goes to show how challenging it is to impose order and a “conceptual roadmap” on this area of the literature.

        What I’d hope you, and other readers, would take away from my post would be that, *on their own*, some classic ideas about the IDH either don’t work at all (idea #1 in the post), or don’t work at all the way their authors thought because they don’t actually identify any effect of FLUCTUATIONS, as opposed to merely effects of long-term average environmental conditions (ideas #2 and 3 in the post). As you note, it is sometimes true that one can append to these classical ideas other ideas, and the combination then works. For instance, temporal fluctuations in relative fitness (Hutchinson 1961) are necessary, but not sufficient, for a storage effect. So if you like, you can think of Hutchinson’s (1961) idea as being *part* of Chesson’s storage effect idea. Just so long as you recognize (which many people, including textbook authors, have not recognized) that Hutchinson’s idea on its own is not sufficient, and in fact in his model fluctuations per se have no effect at all. For that reason, Hutchinson’s idea is *not* best thought of as “the core” of the storage effect, or “basically the same thing as” the storage effect, or “kind of like” the storage effect. Thinking that way will only lead you to make mistakes, including misinterpreting real-world data.

  5. […] a new blog to which my friend Jeremy Fox is a primary contributor. Many of his posts are fairly ecology-specific, but some are remarks applicable to science in […]

  6. […] This post is inspired by an honest and good-humored comment by Robin Svensson on my post on zombie ideas in ecology. Robin, by his own admission, is a zombie—he stills sees value in classical theoretical ideas […]

  7. […] coexistence even when there are no temporal niches in the usual sense. Yet another reason why Hutchinson’s zombie ideas about temporal variability and coexistence deserve to be killed off.  Note that this talk may be […]

  8. […] Miller explained why the intermediate disturbance hypothesis is a zombie idea, though he was far too polite to use those […]

  9. […] paper. It’s the kind of thing that might work as a deliberately-provocative blog post (and I certainly approve of those). But as a serious critique of adaptationist thinking, or even as a serious critique of bad […]

  10. […] colleague of mine here at Calgary read my post on how the intermediate disturbance hypothesis is a zombie idea, and decided to stop teaching the IDH to undergraduate ecology students. […]

  11. Robin says “I cannot do so clever reasonings, but I do observe the intermediate disturbance hypothesis in nature”. The problem is that Jeremy (and Chesson) and Simon use two completely different meanings of the word disturbance, both present in literature. The first – temporal variability of factors – is perhaps the more widespread; the second is what Tilman calls “loss rate”, or Grime’s of disturbance: “total or partial destruction of biomass”. The second has no teemporal variability, there are only “bad years” , so the reasoning of Chesson doesn’t apply; in such cases the environmental conditions are simply no more suitable for some species. For instance (a similiar example is in Begon Harper Toewnsend) if you trample on snails, the larger snails will be destoyed and only the little snails (a functional groups that is usually more diverse) will remain. I dont’ know what whas the meaning of disturbance in the Hutchinson’s papers.
    The 1:1 map is in a tale by Jorge Luis Borger, not in the science-fictioner Lem.

    Giuliano

    • It is true that much writing on the intermediate disturbance hypothesis is ambiguous about what is meant by disturbance. However, much is not (Huston 1979 for instance). This illustrates the value of mathematical models: they cut down ambiguity.

      Thank you for the correction on Borges, my memory must really be going to have confused Borges and Lem 😉

  12. Dear Jeremy,
    interesting and thought provoking post. I was, however, somewhat confused about some of your zombie arguments. I have detailed these confusions on my own blog, because I was afraid that the putting all my thoughts as a reply would not be extremely legible. I am looking forward to your thoughts on my confusion, and hopefully you can show me where I went wrong.

    http://www.cottenielab.org/2011/09/idh-as-zombie.html

    But this is fun, it has been a long time since I spent so much time thinking about IDH, and how to explain it to myself, let alone to students. It is good to be challenged on my assumptions. I am looking forward to some of your other ecology zombies!

    Karl

  13. […] Cottenie has a thoughtful post up responding to my post on the zombie idea of the intermediate disturbance hypothesis. That’s what I was hoping to do: get people to stop and think, so I’m really glad Karl […]

  14. […] of course: zombie ideas in ecology Eco World Content From Across The Internet. Featured on EcoPressed Opower and Honeywell […]

  15. […] but the Oikos blog is the home of zombie ideas in ecology. For “gonzo” ideas in ecology, go here. Share this:FacebookLike this:LikeBe the first […]

  16. […] valid and testable mathematical models. It didn’t arise from logical fallacies like the IDH, or over-literal interpretation of mathematical models like r-K selection. For that reason, […]

  17. […] post on how the intermediate disturbance hypothesis is a zombie idea has garnered more pageviews and generated more discussion than anything else I’ve written for […]

  18. I just found this blog yesterday, and it is of great interest to me because i am currently writing a Canadian edition of a second year Ecology text. Like most, it covers the intermediate disturbance hypothesis; and like many of the unenlightened zombies of which you speak, i find that its core idea has applicability to the kind of environments in which i work (boreal forests). I don’t take it as gospel but frankly i find it less zombie-like that many other core ideas in ecology, like limited similarity (surely more of a zombie idea than IDH) and the competitive exclusion principle itself. I am aware of non-linear, non-additive effects; i am aware of the storage effect; but i, like Robin, find that there are many real-life (I.e. non-model) ecological situations in which disturbance does keep systems in a kind of non-balance that does indeed create opportunities for some species and provide a “breather”, so-to-speak, for others.

    My particular concern is this: the difficulty of conveying the current state of ecological theory in a way that is comprehensible to the typical undergraduate student. You simply can’t hit them with mathematical models at every turn; you have to explain things to them in a way that is logical, yes, but also simplified and coherent. In regards to IDH, for example, i am presenting it; showing some examples where it seems to apply and others where it doesn’t, and encouraging students to consider it critically; but no way am i going to “throw the book at it”. My larger purpose in the treatment of competition is to divorce their minds from what is to me a far more dangerous predilection–namely, the assumption that competition is the major structuring force affecting community structure. I want them to appreciate how many factors allow and indeed promote co-existence–not just fluctuating environments, not just niche shifts, not just greater intraspecific competitive pressures, but also indirect interactions, interspecific mutualisms (direct and particularly indirect), predation, etc, etc. The storage effect will be part of that discussion of course. Any ideas on how to juggle the desire for comprehensiveness with the need for clarity in a second year text would be more than welcome!

    • Thanks for thoughtful comment Isobel. I think it’s great that a textbook author is thinking about this stuff, and I’m flattered to be asked for my thoughts on how to convey this stuff to undergrads.

      First, I agree 100% that zombie ideas about the IDH aren’t the only zombie ideas we perpetuate to undergraduates. Limiting similarity, at least the way it’s usually taught to undergraduates, is probably another.

      I wouldn’t say the competitive exclusion principle is a zombie, though. The conditions required for it to hold simply rarely or never hold in nature. Which doesn’t mean the principle is irrelevant, any more than, say, the Hardy-Weinberg law is irrelevant to genetics, or models of exponential growth are irrelevant to population biology. The importance of the competitive exclusion principle is that it gives us a baseline, so that we can ask questions about the causes of deviations from that baseline. I teach the competitive exclusion principle, but not because I think it usually or even often holds, but because an effective way to make sense of how the complex real world works is to first understand how a simple, hypothetical world works. If you want to understand coexistence mechanisms, you have to understand what the world would be like if there weren’t any coexistence mechanisms. To understand density dependent population growth, you first have to understand density-independent population growth. To understand the consequences of assortative mating for genotype frequencies, you first have to understand random mating (Hardy-Weinberg). Etc.

      I also absolutely agree that undergraduate textbooks need to simplify key ideas–I absolutely do not advocate filling our undergraduate textbooks with lots of advanced mathematical models. But I do think there is a difference between simplifying sophisticated ideas, and presenting simple but incorrect ideas.

      So, what should a textbook tell undergraduates about the consequences of disturbance, and fluctuating environmental conditions, for coexistence? I don’t know that this is a complete answer, but here are some suggestions:

      I think you start with the observation that disturbances, and more broadly fluctuations in abiotic conditions, are ubiquitous on all spatial and temporal scales. So we need to think about the consequences of this, but it’s not immediately obvious what the consequences are. For instance, will disturbance and environmental fluctuations allow more species to coexist than could coexist in their absence? Or will disturbance and environmental simply change the identity of the winning species, so that the species that competes best in disturbed or fluctuating environments eliminates the others? Or will disturbance and environmental fluctuations perhaps not have much effect at all–just a bit of “noise” superimposed on the major trends or patterns which are created by other factors? In fact, all three possibilities can occur, depending on the nature of the disturbance or environmental fluctuation, and of the community experiencing those disturbances and fluctuations (a fact one could easily illustrate with empirical examples).

      Then, having introduced the range of empirical observations that we want to explain, move on to the possible explanations. Here, I do think it’s important to clearly distinguish between empirical observations and patterns, including the results of experiments, and the causal explanations for those results, even in an undergraduate textbook. Failure to draw this distinction in the context of the IDH is a big reason why zombie ideas about the IDH persist. As I’ve noted in previous posts and comments, it’s certainly the case that in some systems (although only a small minority of systems, according to the review by Mackey & Currie) diversity peaks at intermediate frequencies or intensities of disturbance (either naturally-occurring, or experimentally-imposed disturbance). But as I’ve explained, that is simply not evidence for zombie ideas about the IDH, which are zombie ideas about the causes of that pattern. In the context of the IDH, lots of professional ecologists seem to think of the empirical pattern of diversity peaking at intermediate disturbance, and the zombie ideas proposed to explain that pattern, as almost one and the same, as if the explanation of the pattern was so obvious that the pattern itself somehow implies the explanation. So, with all due respect, when you say that you think there really are many real-life situations in which disturbance, merely by creating a “non-balance”, promotes coexistence by somehow providing a “breather”, “so to speak”, I’m afraid you are simply incorrect, or at least speaking too ambiguously. You are misinterpreting, or at least speaking too ambiguously about, “real world” causes. The storage effect, etc. are real world causes. The three zombie ideas I refuted in my post do not occur in the real world, or even in a simple hypothetical world, because they are logically flawed, just as there is no world, real or hypothetical, in which 2+2=5.

      So, how do you teach students non-zombie ideas about the effects of disturbance on coexistence, without doing math? Well, you have to use words to summarize the math–but you have to use the right words, and summarize the right math. For instance, I could absolutely see structuring all of your discussion of coexistence mechanisms–not just disturbance, but all causes of coexistence, like keystone predation, differential resource use, etc.–around Chesson’s ideas of equalizing and stabilizing mechanisms. You don’t need any fancy math to convey these ideas. At the broadest-brush level (and even an undergraduate text could be more elaborate and precise than this), what the math says is that, in order for competitors to coexist in the long run, you have to have two conditions hold. First, the competitors have to make their living in at least slightly different ways, so that they compete more strongly with members of their own species than with members of other species. Second, insofar as they do make their living in the same way (e.g., share the same food sources), no one competitor can be too much better at living in that way than the others (that’s the equalizing bit). For instance, if two competitors overlap a lot (but not completely) in the foods they eat, but one is way better at competing for those shared foods than the other, the inferior competitor can still get excluded even though it has some foods all to itself.

      Those two general principles always hold, in the real world, if you look at things in the right way. So you can use them as an overarching framework in which to organize discussions of every coexistence mechanism you want to discuss. That sort of overarching framework seems like a desirable thing for a textbook, so that students aren’t just faced with a mass of special cases and no way to link them all together. For instance, keystone predation (predation that falls disproportionately heavily on the best competitor) is an equalizing mechanism–by inflicting additional mortality on the best competitor, you reduce the superiority of that species relative to its competitors (keystone predation can be stabilizing too, of course, for reasons that are a little harder to explain). As a second example, spatial variation is stabilizing–if plant A is the best competitor in wet areas, and plant B is the best competitor in dry areas, then in a landscape with wet and dry patches, they can coexist, because each will be found primarily in the patches where it grows best, and so will experience strong intraspecific competition but weak interspecific competition. Spatial variation is also equalizing in the sense that, if the entire landscape were wet, species A would just be superior to B. So even if A and B were spatially-separated on a wet landscape, and so competing mostly intraspecifically, that wouldn’t be a stable state of affairs–species A would eventually take over. Even if the landscape was mostly wet rather than entirely wet, this still might be too unequal a situation for species B to persist–the few dry patches might get swamped by propagule pressure of species A from the huge wet patches.

      With regard to effects of fluctuating conditions, I actually think one could even use Hutchinson’s zombie idea about environmental fluctuations as a baseline, much like the competitive exclusion principle, to reveal to students what needs to be the case for environmental fluctuations to generate coexistence. Contrary to what Hutchinson thought, you don’t get coexistence simply because the environment favors one competing species some of the time, and another competing species some of the time, no matter what timescale on which the environment fluctuates. The reason can easily be made intuitive without doing any fancy math–e.g., if the environment favors one competitor 99% of the time, and the other 1% of the time, and all else is equal, who do you think will win in the long run? Put like that, the correct answer is obvious. And while you would get coexistence if the environment favored each competitor by exactly the same amount, exactly 50% of the time how likely is that, really? (answer: not too damn likely) So, for environmental fluctuations to promote coexistence, it’s not enough for them to just favor different species at different times. With that in mind, you can segue into a verbal summary of, say, the storage effect (which can be summarized verbally at a level suitable for undergrads–see for instance the Wikipedia page I linked to in a previous post. I actually do think the storage effect can be summarized in a single math-free paragraph, in a way that makes clear it’s not at all the same as zombie ideas like Hutchinson’s).

      Similarly, with regards to effects of disturbance (by which I mean discrete, density-independent mortality events), you could certainly tell undergrads that disturbances that affect all species the same way (as in Huston 1979) are equalizing but not stabilizing, because they reduce every species’ growth rate and so reduce the difference in growth between superior and inferior competitors. Importantly, continuous mortality that affected all species equally (e.g., continuous, unselective mowing or grazing of competing plants) would be equalizing for the same reason, which illustrates that Huston-type unselective disturbance works not by “interrupting” anything, or by providing a “breather” for any species, but simply by making life harder on everyone (if everyone is growing poorly on average, no one can be growing all that much faster than anyone else). So Huston-type disturbance (which is the simplest baseline case) isn’t stabilizing, and so on its own would at best lead to slow competitive exclusion. Which could segue into a discussion (which could be as short as a paragraph, I think) of how disturbance could be stabilizing (e.g., a verbal summary of “successional niches”).

      The above is pretty off the cuff–hope it’s helpful. Happy to correspond further via email if that would be more useful. Obviously there are larger issues here, such as how much space to devote to disturbance vs. other topics, and more broadly to coexistence vs. other topics, which are going to shape what you want to say and how you want to say it. In offering the above comments, I obviously can’t really account for those larger issues.

  19. Thanks for the input. I agree that the CE principle works well as a default; the problem is that it is rarely framed in that way but rather as a mantra that becomes trivialized in its application. Hence the need for synthesizing niche and neutral perspectives.

    On the disturbance front– I get your/Chasson’s argument re disturbance not eliminating the impact of competition on community structure in general and diversity in particular. I’ve never been ready to go to the wall for the IDP as a principle, though i do see it as having utility. But it seems to me that Chasson’s position about what happens after a disturbance fails to take sufficient account of factors other than competition that affect diversity by affecting persistence and/or colonization. Focusing so exclusively on the impact on relative growth performance (as Chasson does) seems to me a reasonable position where competition involves mechanisms such as overgrowth and consumption in highly productive habitats such as fertile grasslands in temperate sites.

    Does it apply as well to less productive habitats where faster growing species may continue to be “winning” a competitive interaction with another species after a disturbance, but be at increased predation risk from generalist herbivores with a propensity to switch to fast-growing species? or where faster-growing species may be more prone to ongoing abiotic stresses that prevail in the post-disturbance habitat, such as desiccation risk or greater extremes in winter low temperatures?

    It seems to me that these other factors are particularly potent in infertile ecosystems in the harsh climates of northern latitudes, where fast growth (at least in plants) is rarely the determining trait of success. In the boreal forest, it is often about hanging-on and competing by making efficient use of resources while protecting against abiotic stresses, not rapid growth. Mutualistic relationships both with unrelated species and even with species that might be competitors under more favourable conditions take on increasing importance through neighbourhood amelioration. Think the “wood wide web” wherein individuals of different tree species of similar niche requirements are linked by their mycorrhizal networks. In this situation, a disturbance might indeed not make exclusion due to competition any less likely, as Chasson claims, but simply because it wasn’t very likely in the first place. Nor is the storage effect–as powerful as that concept is in many environments–likely to have as much impact on co-existence as in a more favourable environment exposed to disturbance.

    Perhaps it comes down in part to what another blogger mentioned about the different senses of “disturbance” being confounded in this discussion. I don’t think ANY principle (or less lofty than that, any mere generalization) about disturbance and diversity is likely to apply to a range of disturbances AND to fluctuating conditions AND to harsh conditions. There are so many permutations and combinations of all those realities.

    I thank you for your suggestions on tackling some of these topics in a textbook context. It is a daunting task, particularly when space constraints are so intense. I will most definitely take them into consideration.

    • Dear Isobel,

      Thanks for your further comments. You’ve raised some issues that many correspondents have raised with me, so I want to reply at length, as I think many will find your comments, and my reply, useful.

      In your comments on the scope of applicability of Chesson’s ideas, I think you have misunderstood his ideas. I don’t mean this as a criticism–I think everyone who reads his work initially struggles to fully appreciate his point. Let me try to help clarify.

      “Relative growth performance” is always and everywhere the only thing that determines relative abundance. How could it be otherwise? How could one species increase in abundance relative to another, except by growing at a higher per-capita rate than the other? You seem to be confusing Chesson’s general concept of relative growth performance (which is essentially the same thing as “relative fitness” in evolution), with the much more narrowly-applicable concept of one species overgrowing another, or perhaps taking up resources that could otherwise have been taken up by another. Further, when Chesson talks about “competition”, he means competition in the broad sense emphasized by Darwin in the Origin: not just exploitative or interference competition, but any direct or indirect interaction between species that causes one to increase in relative abundance at the expense of the others. For instance, two species can be direct or indirect mutualists, in the sense of increasing each others’ absolute fitness, and yet one can exclude the other (have a higher relative fitness, and so eliminate the other). The “wood wide web” need not promote coexistence! And “coexistence mechanisms” are any mechanisms that allow species, if they become rare, to bounce back.

      So I’m sorry, but I respectfully disagree if you think there are no general principles here–there are. But recognizing their generality requires recognizing the level of abstraction required to purchase that generality. I think that’s what you’re struggling with (and you’re not alone!) If you want to say something completely general about coexistence mechanisms–and that’s what Peter Chesson’s work does–you have to define your terms in a completely general, and thus very abstract, way. You have to talk, not in terms of “exploitative competition” or “disturbance tolerance” or “mutualism via mychorrhizal networks”. Rather, you have to talk in terms of completely general concepts like “relative per-capita (or for some organisms, per-unit biomass) growth rate”, “relative abundance (or for some organisms, relative biomass)”, and “ability to increase when rare”, which apply universally. Then, within that maximally-general framework, you can talk more specifically about how, in some systems, exploitative competition and resource use differentiation are key determinants of relative per-capita growth rate and ability to increase when rare, whereas in other systems tolerance of “abiotic stress” or the ability to exchange resources with mutualistic partners are key determinants of relative per-capita growth rate and ability to increase when rare.

      Even the “storage effect” is actually a very general kind or class of coexistence mechanism, which can be produced by many different underlying biological mechanisms, and so is likely to apply much more broadly than you seem to think is the case. For instance, annual plants (which have a seed bank), perennial plants and many animals (which have long-lived adults), many freshwater microbes and plankton (which have resting stages or eggs), and many other kinds of organisms all have the potential to coexist via a storage effect, despite the fact that they occupy very different environments (ranging from unproductive deserts to productive forests and eutrophic lakes) and “store” the gains from good periods of population growth via different adaptations.

      Whenever anyone says to me that there are no completely general theories in ecology, because the world is too complicated, I like to remind them of a completely general theory, about an equally-complicated subject, which they all believe wholeheartedly: evolution by natural selection. It is the case, for every organism that ever has or ever will live, that if it exhibits heritable variation in traits affecting fitness, those traits will evolve via natural selection. The theory of evolution by natural selection is completely general because it is framed in generally-applicable, abstract terms. Every organism has “traits”. Every organism has “fitness” (roughly, the ability to survive and reproduce). Every organism exhibits “heritability” (for some reason or other, offspring tend to resemble their parents). Etc. It’s not that the theory only applies to, say, Darwin’s finches, but not to, say, bacteria. Finches and bacteria have different traits (e.g., beaks vs. cellular biochemistry) subject to different selection pressures (e.g., selection to eat seeds of a certain size vs. selection to resist antibiotics) which are passed on in different ways (e.g., sexual vs. asexual reproduction). But the theory of evolution by natural selection applies to both. Chessonian coexistence theory is the same way. If you think it only applies in certain contexts, you’ve misunderstood it. Just as you’ve misunderstood the theory of evolution by natural selection if you think selection can only arise from exploitative or interference competition (a misunderstanding Darwin himself was keen to refute). I have old posts on this blog that talk more about this.

      I absolutely agree that it’s a challenge to get this perspective across to second-year undergrads. But I don’t think it’s impossible. In every area of science, or probably any subject, we as educators are always faced with the challenge of how to convey general ideas without the student confusing specific examples with the general ideas. I think evolutionary biologists manage to square this circle, so I think ecologists can too. I think it’s great that you’re thinking of giving it a shot.

  20. oops, make that Chesson…

  21. […] the previous post I asked readers if a post of mine had changed their minds about whether the intermediate disturbance hypothesis is true or even […]

  22. […] Zombie ideas in ecology […]

  23. I thought the intermediate disturbance hypothesis inherited the idea of a climax community. Sometimes it takes a zomie to kill a zombie. But maybe I’m mistaken and the climax is as alive and kicking as the intermediate disturbance.

    P.S.: It might also be interesting to collect fossil ideas and paleologisms (neologisms gone fossil), that is, terms and concepts that have really gone extinct from usage.

    • Hmm…can you give some citations linking the IDH to the idea of a climax community? Personally, I’ve never really thought of the IDH in general as having much of a connection to the idea of a climax community, which is of course an idea from the succession literature. Although there certainly are specific ideas about how disturbance affects community dynamics that link to the succession literature. For instance, Pacala & Rees’ (1998) model of successional niches is basically a model of what happens if you impose disturbances on a system that, if undisturbed, would follow a particular kind of successional trajectory. And I suppose if you want to define a “climax” community as any community that’s at a stable equilibrium, then you would interpret Huston (1979) as claiming that disturbances promote coexistence by preventing the attainment of “climax”. But as far as I can recall (sorry, too lazy to go back and re-read), Connell (1978), Huston (1979), and Hutchinson (1961), which are the three classic sources for key (zombie) ideas about the IDH, don’t explicitly talk about climax communities at all. So if there’s a broader or deeper link between climax and the IDH, it’d have to be pretty indirect and implicit, I think.

      In terms of fossil ideas, most of Clements’ elaborate terminology is long since extinct, although the spirit still lives on in phytosociology (does the field still call itself that?) and its predilection for producing “vegetation classification schemes” (e.g., trying to classify the “types” of plant community in N. America). As to whether “climax” is a fossil idea, I’m not sure, I don’t have much occasion to read the recent forest ecology and succession literature, but I doubt its entirely extinct the way much of Clements’ terminology is.

  24. didn’t mean a direct connection, just that the demise of one theory about large scale ecosystemic dynamics leaves room for another.

    • Ah, ok. In that case, I wouldn’t say that the IDH per se was a major cause of the decline or demise of the notion of climax communities.

  25. Yeah, but the IDH Zombie might go away, once an alternative grows up. Hopefully, that one will turn out to be truly alive.

    • One can only hope! Well, hope, and keep making zombie jokes in the meantime, in an effort to speed things along. 😉

  26. […] my original zombie ideas post, I criticized three distinct theoretical claims about how disturbances and fluctuating […]

  27. […] absence of much data, or even despite a pretty clear-cut empirical consensus—with the history of the intermediate disturbance hypothesis, which has never been a very controversial idea despite a horrible empirical track record (much […]

  28. […] most viewed post was, not surprisingly, “Zombie ideas in ecology“, with 1460 views (including syndicated views). That was also the most-commented post (39 […]

  29. […] when, because of confirmation bias, those studies are the least-reliable ones. You wonder how zombies first arise? This is […]

  30. […] think this is a big part of why zombie ideas about the intermediate disturbance hypothesis are so hard to kill. You can summarize zombie ideas about disturbance, and correct ideas about […]

  31. […] testing the intermediate disturbance hypothesis (IDH). Which, as readers of this blog know, is a really, really unfortunate example. Experiments to test predictions are only as good as the predictions they purport to test. So if […]

  32. […] Note as well that all those attempts to change the question were actually tried by commenters on my original zombie ideas post, or folks who’ve corresponded with me privately. The Professor in this post is just trying to […]

  33. […] are famous ecologists like Nick Gotelli who know a lot about statistics. Because famous ecologists never make mistakes. Nope, never.* Also interesting to see the same commenter imply that, by publishing his criticisms […]

  34. […] discussion in detail, I believe that this is the physics version of what Jeremy Fox calls a “zombie idea” – it originates from a historical fallacy that was made in the early days of this […]

  35. […] many of the most serious mistakes in ecology arise from insufficient attention to detail (see here and here for just two of many possible […]

  36. Great zombie ideas 🙂

  37. […] gone on a zombie killing spree, started by a blog post of Jeremy Fox here at the Oikos blog (link here). Dr. Fox defined zombie idea as having “survived decades of attacks from the theoretical and […]

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    you, I certainly get irked while other people consider worries that they just don’t realize about. You managed to hit the nail upon the top as neatly as defined out the whole thing with no need side effect , other folks can take a signal. Will probably be back to get more. Thanks

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  40. […] field has its ‘zombie ideas’, ideas based on disproved notions (and so are not ‘alive’), but whose influence […]

  41. […] Ecological synthesis is tricky. One of its many challenges is that empirical data rarely paint a clear picture either supporting or refuting a given hypothesis. More typically, empirical studies have diverging results. But even for hypotheses where refuting evidence is overwhelming, ecologists are often reluctant to abandon them (see Oikos Blog on Zombie Ideas). […]


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