Objections to microcosms in ecology, and their answers

I work in protist microcosms. A typical experimental unit is a glass jar with 80 ml of nutrient medium, which I inoculate with bacteria, protists, and perhaps other microbes. Then I (actually my research assistants) follow the resulting population dynamics. Several features of this system combine to make it an excellent model system for asking fundamental questions about population and community dynamics. Protists have very short generation times (4-48 h), so you can collect hundreds of generations of data in a few months. Microcosms are easy and cheap to replicate highly, giving you a lot of statistical power. You can control and manipulate features of the system that are difficult or impossible to control and manipulate in most other systems. I tend to use the system to ask questions about the consequences of particular processes or combinations of processes that would be difficult or impossible to ask in other systems. For instance, how does productivity, in isolation from other factors, affect the occurrence of alternate stable states and assembly cycles (Fox 2008 Oikos)?

The advantages and drawbacks of protist microcosms, and of artificially-assembled communities more generally, have been debated in various places (see, e.g., papers in the April 1996 issue of Ecology and chapters in Bernardo and Resetarits (eds.) 1998). But over the years I’ve run into various objections that either haven’t been addressed publicly, or haven’t been addressed in quite the way I’d address them. Plus, although the debate over microcosms seems to have died down a while ago, who knows when it will flare up again, so I figured I might as well take a preemptive shot in the next Microcosm Wars.

So below are some objections to microcosms (in bold), and my own answers. I emphasize that I really have encountered all these objections (sometimes in unsigned reviews, so I can’t link to the sources); I’m not setting up straw men here. I also emphasize that, in answering these objections in the way I do, I’m speaking only for myself. Microcosm experiments are conducted for different reasons by different people, who would probably have different answers to these objections. Indeed, one overarching problem I have with these objections is that they’re blanket objections, and those who raise them often don’t seem to pay attention to the various quite distinct reasons why microcosm experiments are conducted.

I should also note that microcosms absolutely have their limitations. There are plenty of questions you just can’t ask using microcosms. For instance, protists lack stage-structure, so you can’t study stage-structured population dynamics with protists. Protists and other small organisms aren’t convenient for collecting individual-level data, and so if you want to scale up from individual-level data to population dynamics you need a different system (I understand that this is why my fellow Oikos editor Andre de Roos switched from working on zooplankton to working on fish). It’s hard to study the bacteria in a typical protist microcosm, which means I (like many ecologists) mostly treat the bacterial portion of the system as a ‘black box’ whose effects I hope I can summarize implicitly (e.g., by treating bacterivorous ciliates as growing logistically, rather than actually modeling their interactions with the bacteria). But those kinds of detailed considerations are of a very different character than the blanket objections to microcosms which I discuss below.

Microcosms just use organisms to solve equations. Yes, but so do non-microcosm systems. Anything can be described with equations, and so all organisms can be said to ‘solve equations’. The challenge in microcosms, just as in any other system, is to figure out what equations the organisms are solving, at least to a sufficiently good approximation to answer the scientific question of interest. (And if you insist that your system is so complex that it can’t be described with equations, how do you know humans can comprehend it?)

Microcosms are rigged; the results can’t help but confirm the theory. Boy, I wish that were true! Believe me, if I could rig my experiments so they always came out the way I wanted them too, I totally would (and my cv would look a lot more impressive!) I can actually see where this objection comes from, because there certainly are microcosm papers which report such clean results, conforming so beautifully to theoretical expectations, that it’s hard for someone who doesn’t work in the system to believe the experiment wasn’t somehow ‘rigged’. Gause’s (1934) competition experiments are famously well-described by the Lotka-Volterra competition model, and Kaunzinger and Morin’s (1998) test of food chain theory is a terrific recent example. But those kinds of theory-confirming papers not only aren’t rigged (more on that in a second), they’re far outnumbered by theory-disconfirming papers. You know how I just said that, in microcosms, the challenge is to figure out what equations the organisms are solving? Well, that’s a big challenge, because it’s often not the equations you thought they were solving. Take it from me, even though protists aren’t animals, they definitely obey the Harvard Law of Animal Behavior (‘under carefully controlled conditions the animal does what it damn well pleases’). For example, see Harrison 1995 and Fox 2007, to pick just two of many possible examples. Hard as it may be to believe for people who don’t work in microcosms, they do have the capacity to surprise. They can reveal new phenomena and unexpected behavior (e.g., effects of species loss on food web connectance in Fox and McGrady-Steed 2002; effects of dispersal on within-patch demography in Fox 2007). That capacity for surprise is what makes them useful. Microcosms are complex enough to surprise, but simple (and controllable, and replicable) enough that the source of the surprise hopefully can be identified. If your system is hugely complex and ‘noisy’ (which is often shorthand for ‘hugely complex’), it can be hard to tell if you’ve been surprised or not, because of the many factors that can obscure the signal you’re looking for. It can be even harder to figure out why you’ve been surprised. By throwing up ‘tractable surprises’, microcosms can suggest new ideas and teach us new things, not just serve a negative role as a first-cut test of theory. ‘If a theory doesn’t work in microcosms, it won’t work anywhere’ is a claim sometimes used to justify microcosm experiments, but it’s not a claim I personally buy (I used to, but not anymore).

And even when microcosms do conform to theoretical predictions, well, that’s generally a surprise too. Because microcosms never conform precisely to theoretical assumptions—that’s pretty much impossible. So even when the theoretical predictions are supported, the experiment demonstrates that those predictions are robust to the ways in which microcosms violate the relevant theoretical assumptions. For instance, Kaunzinger and Morin (1998) is a beautiful confirmation of Oksanen et al.’s (1981) predictions for how equilibrium biomasses on different trophic levels change along a productivity gradient—even though Kaunziner and Morin’s population dynamics were highly non-equilibrial (they averaged over a predator-prey cycle), even though their top predator seriously violated the assumption of a linear functional response, even though their basal trophic level in some treatments comprised a heterogeneous mixture of bacteria rather than the single species assumed by Oksanen et al., and even though their unshaken microcosms violated the assumption of a spatially-homogeneous system. Indeed, theoretical models that explicitly incorporate precisely these complications actually make different predictions than Oksanen et al. So a very interesting question is why the Oksanen et al. predictions are robust to these complications. One way to get at that question would be to manipulate features of the system like the number of species per trophic level and the spatial homogeneity, and indeed such manipulations have been conducted (e.g., Fox 2008 Oikos, Fox and Barreto 2006). I suspect this objection gets raised because my fellow microcosmologists and I often emphasize the ways in which our system conforms to theoretical assumptions while neglecting to emphasize the ways in which it doesn’t.

Microcosms aren’t ‘realistic’ or ‘natural’. I can totally see the point of this concern if (and only if!) the goal of a microcosm experiment is to mimic some specific natural system, or some specific feature of some specific natural system. For instance, if you put an individual predator and some prey in a small container in order to estimate the predator’s feeding rate in nature, you’d better be sure that the container doesn’t introduce any artifacts which bias your measurements (e.g., lacking prey refuges which exist in nature). This is the main reason why Carpenter (1996) objects to microcosms. But if that’s not the goal of the microcosm experiment, then this objection is simply irrelevant and frankly it frustrates and mystifies me when it’s raised. I wonder if those who raise this objection have really thought it through, and ask that they consider the following points:

a. In many respects, microcosms are realistic. For instance, all microcosm experiments use species found in nature, and most use species that coexist in nature. Nobody uses robots, or Jurassic Park-style lab-created species, or children pretending to be animals (but see Bell 2007). And the resulting dynamics are realistic in many respects too. For instance, the average strength of trophic cascades in protist microcosms is almost frighteningly similar to the average strength of trophic cascades in nature (Fox 2007 Oikos). Protist microcosm food webs exhibit pyramids of numbers and biomass, just like many natural food webs. Etc.

b. Sure, microcosms aren’t exactly like any specific natural system. But neither is any other natural system! As every ecologist surely knows, natural systems differ a lot from one another, and change over time. ‘Natural’ isn’t one state of affairs, it’s a massive range of states of affairs. So if you say microcosms aren’t natural, which natural system are you comparing them to? And don’t say ‘they’re unnatural compared to every natural system that’s ever existed or could exist’. No one knows what sort of natural systems could exist, and more importantly protist microcosms actually are reasonable analogues for small, naturally-occurring water bodies such as puddles and rockpools (McGrady-Steed and Morin 1996).

c. Many microcosms aren’t intended to be realistic or natural. Again, the point of my experiments is not to reproduce the behavior of any particular natural system, it’s to obtain information that couldn’t be obtained in any other way. Criticizing this kind of experiment as ‘unnatural’ is like criticizing a car because it can’t fly.

d. No experiment is ‘natural’ or ‘realistic’. That’s the whole point of experiments, including field experiments—to change nature, to create conditions that wouldn’t otherwise exist, i.e. unnatural conditions. We do that because a really good way to obtain information about how realistic systems work is to create unrealistic conditions.

e. You’re effectively insisting that we discard useful information which we could not obtain in any other way. Microcosms, by allowing you to create conditions which would be difficult or impossible to create in nature, allow you to expand your information base. For instance, it’s really useful to know that, under the conditions produced by Kaunzinger and Morin (1998), the Oksanen et al. model works. It mostly doesn’t work under other conditions, so comparing the systems where it does work to the systems where it doesn’t lets you develop testable hypotheses about the circumstances under which it works or doesn’t work. You wouldn’t be able to make such comparisons if all you had were systems where the model doesn’t work. So if you don’t think we should do microcosm experiments because they’re ‘unrealistic’, you’re effectively saying that you want less information, about a smaller range of systems and conditions. Please explain how that could possibly be a good thing! And don’t just explain it to me, explain it to Charles Darwin. Charles Darwin, the greatest naturalist in history, didn’t just rely on observations of unmanipulated nature for evidence for evolution by natural selection. One of his most important lines of evidence, the line of evidence with which he chose to begin the Origin, was the effects of artificial selection in domestic species. Artificial selection provided Darwin with evidence relevant to interpreting nature and testing his hypotheses, evidence that he could not have obtained any other way, even though artificial selection as practiced by breeders is highly unrealistic. For instance, selection coefficients imposed by breeders often are much stronger than those typically observed in nature, and breeders often select for traits that would never be favored in nature. My point here is not proof by authority; Darwin wasn’t infallible. My point is merely to ask those who have a blanket objection to all microcosm experiments as ‘unnatural’ or ‘unrealistic’ (e.g., Carpenter 1996) to carry their arguments to their logical conclusions.

f. If there’s some specific respect in which you think microcosms are unrealistic, it’s probably possible to manipulate that feature of the system and thereby turn your objection into a testable hypothesis. A constant, undisturbed environment is unrealistic? Ok, let’s manipulate environmental variation or disturbance (e.g., Warren 1996 Oikos, McGrady-Steed and Morin 1996 Oikos, Fukami 2001 Oikos). It’s unrealistic to mix species with no coevolutionary history? Ok, let’s manipulate coevolution (see, e.g., the work of Mike Brockhurst, among many others). It’s unrealistic for a community to be closed to immigration and emigration? Ok, let’s open it to dispersal (e.g., Holyoak and Lawler 1996, Warren 1996 Oikos). Etc.

Microcosms are too small-scale. Umm, you are aware that protists are really tiny, right? Population sizes in my microcosms are on the order of 10,000-1,000,000, which is as large or larger than the population sizes in the study areas most ecologists use to study  most macroscopic organisms (e.g., there are only 225,000 trees in the famous 50 hectare plot on BCI). So relative to the size of the organisms, microcosms are actually large-scale (and long-term, relative to the generation times of the organisms). And unshaken microcosms contain substantial spatial heterogeneity at spatial scales relevant to microbes (e.g., Meyer and Kassen 2007). Plus, spatial scale can be manipulated, for instance by manipulating vessel size, and by studying arrays of microcosms linked by dispersal (e.g., Holyoak and Lawler 1996).

Microcosms lack the full range of processes that occur in nature. The objection here, as best I can understand it, is that a system that includes only a subset of whatever goes on in any natural system cannot tell us anything useful about nature. Rather than extending our information base, microcosms just represent irrelevant ‘apples’ that can’t usefully be compared to natural ‘oranges’. Again, if the objection is only meant to apply to microcosms that try to mimic specific natural systems, then I can appreciate it. But if it’s meant to apply more broadly, then I don’t buy it at all, because it amounts to denying that ecologists can build up an understanding of how a complicated ecological whole works by studying its parts. Carpenter (1996) claims that studying parts of a system is informative in molecular biology (‘a molecular biologist who isolates ribosomes is working on ribosomes’), but not in ecology (‘an ecologist who isolates organisms in bottles may not be working on communities and ecosystems in any relevant sense’). Unfortunately, I confess I don’t fully understand his reasons for this claim. One of his reasons is that ‘there is general agreement about human health goals that rationalize most of [molecular biology’s] funding’. What this has to do with the scientific validity of ecological microcosms I have no idea. Another is that ‘relatively rapid replicated study is possible at several levels’ in molecular biology, which you would think would be an argument in favor of microcosms in ecology since rapid, replicated experiments are what microcosms are for. The claim that ecologists cannot build up an understanding of a complex ecological whole by studying its parts just strikes me as so obviously false that I don’t even know what to say in response.

Microcosms should not be studied for their own sake. The ultimate goal should be to understand nature. I don’t know anyone who studies microcosms for their own sake. I sure don’t. I mean, yes, I do play close attention to the results of previous experiments in microcosms, in order to help me design my own experiments. But that’s surely no different than what any field ecologist does—you build on what’s already known in order to learn something new. The mere fact that someone conducts a lot of microcosm experiments, and no field studies, is not evidence that he or she is just interested in microcosms for their own sake. I ride the bus a lot too, but I don’t ride the bus for its own sake. A frequently-employed means to an end is still a means to an end, and contrary to Carpenter (1996) I don’t believe there’s any serious risk that that a frequently-employed means will ever be mistaken for an end. Heck, field experiments are only a means to an end, but you don’t see anyone worrying that, if we focus too much on field experiments, we’ll start treating them as an end in themselves. (Come to think of it, maybe we should start worrying about that…) (just kidding)

As an aside, while the ultimate goal of microcosm work, including my own, often is to understand nature, worthwhile work in ecology can have other goals (e.g., Caswell 1988 talks about how theoretical ecology has ‘a life of its own’, independent of empirical data).

It’s irresponsible to train people to do microcosms; to solve real-world ecological problems we need field scientists with a deep appreciation of natural history and a ‘sense of the ecosystem’. Carpenter (1996) says this (and yes, he actually uses the word ‘irresponsible’). I’m glad he says it, because I suspect this gets to the heart of the matter. All the above objections, I suspect, really spring from the feeling that, if you’re not doing it in the field, and if your starting point is not natural history, you’re not doing proper ecology.

If you buy this objection, I doubt there’s anything I or anyone can say to change your mind. But a few remarks are in order.

First, if solving real-world ecological problems is your overriding goal, you should seriously consider going into law, politics, or economics rather than field ecology. The ultimate causes of anthropogenic impacts on the environment are not ecological. And while ecological knowledge is essential for addressing those impacts,  lack of knowledge typically is not among the biggest impediments to addressing those impacts.  But that’s a discussion well beyond the scope of this blog entry.

Second, I personally am a crap natural historian. So the fact that I work in microcosms is no loss to natural history-driven field ecology. 😉 (By the way, this is emphatically not true of everyone who works in microcosms. Peter Morin for instance is an amazing natural historian)

Third, no one I know trains students to be ‘microcosmologists’. Personally, I like to think that I train students to be scientists. For instance, one of my current graduate students entered my lab with a strong interest in working in microcosms, and I steered him towards alpine plant-pollinator interactions because that seemed like a better system in which to address the questions he wanted to address.

Fourth, I can tell you, from my own personal experience, that training students to work in microcosms does not significantly reduce the pool of students who want to train as field ecologists. I struggle to attract graduate students (and undergraduate honors students), and the ones I do attract mostly don’t end up working in microcosms. The vast majority of undergraduates interested in ecology get into ecology because they love the outdoors and wild nature, and they choose graduate supervisors and careers that reflect that love (which I think is great, by the way). Let me tell you, it’s very hard to convince such students to do ecology indoors. If we are indeed, as Carpenter (1996) claims, short on students with the natural history background to do field ecology, it’s not because students who have that background are getting sucked into doing microcosms instead. The students I mostly attract are the rare ones who, although they often love wild nature, also love big, general questions that are relevant to many systems. These students feel, as I do, that if a question could in principle be asked in any system, we may as well ask it in a model system that has features that make it easier to get a clear-cut answer.

Fifth, I respectfully disagree that, in order to solve the world’s ecological problems, and train the next generation of ecologists who will help solve those problems, that we should only train field ecologists. Natural history and a sense of the ecosystem are hugely important, but they cannot answer all the questions we ought to be asking, and indeed can’t even identify all the questions we ought to be asking. For instance, the ideas of alternate stable states, hysteresis, and critical slowing down, which have tremendous management relevance and on which Steve Carpenter himself is currently working, derive from dynamical systems theory and weren’t originally discovered by field ecologists. The competitive exclusion principle, which is implicitly or explicitly part of every field study of competition (e.g., between invasive species and natives) was not discovered by a field ecologist. The many surprising and counterintuitive behaviors of nonlinear, stochastic dynamical systems (e.g., chaos), which are a major plank in the argument for ‘adaptive management’, were not discovered by field ecologists (for instance, think of ‘stochastic resonance’, which may explain outbreaks of many pest insects). The fact that ‘diversity’ does not necessarily promote, and can even inhibit, ‘stability’, was not discovered by a field ecologist (indeed, field ecologists pretty much thought the opposite until Bob May came along). Modeling global climate change and its ecological consequences requires lots of mathematical and computer programming skills that could not realistically be part of the standard training for field ecologists. I could go on, but you get the idea. Good ecology, even good conservation ecology, and even good system-specific conservation ecology, often depends on ideas and skills drawn from other sources than natural history. A ‘sense of the ecosystem’ is necessary but not sufficient to conserve the ecosystem, because ecosystems are far too complex for that.