Passing the mutualism buck: why have theoretical textbooks largely ignored mutualism?

Note from Jeremy: this is a guest post from Christopher Moore. Thank you Chris for writing such a fun and meaty post!


I went to graduate school because I was curiously captivated by a species interaction between plants and animals that disperse their seeds. This interaction is mutualistic; that is, both species directly interact and reciprocally increase each other’s fitness. The animals benefit from the nutrient reward from the plant (e.g., fruit pulp or nut endosperm) and the sessile plants benefit by having the animals do the work of dispersing their seeds across the landscape.

My first semester of graduate school I took one of the best courses of my life, “Advances in theoretical ecology,” whose readings were a mix of current papers and classic papers mostly from Foundations of Ecology by Brown and Real. Although it was an amazing course, I was really surprised that neither the course readings nor the text mentioned mutualism a single time. But what did I know? I was a first-semester graduate student and I thought this was surely an anomalous experience. I thought as I continued my studies I would surely learn more of the theoretical foundations of mutualism.

As graduate school continued, however, this experience was repeated over and over again: I’d go to the library and check out a book or I’d buy a new book with theoretical foci on species interactions, and mutualism would be missing. As examples, I bought Scheiner and Willig’s The Theory of Ecology (2011) the moment it came out (I love the framework of their ’05 paper that preceded it), and despite chapters on competition and enemy-victim interactions (predator-prey, herbivore-plant, host-parasite, etc.), there was no analogous chapter or even a mention of mutualism. I acquired Hastings and Gross’ remarkable 848-page tome Encyclopedia of Theoretical Ecology my final year in grad school. Of the 129 topics there are substantial entries on various species interactions, but not a single mention of mutualism in the entire book.

One day as a postdoc (circa 2016) I was preparing for a talk and decided I wanted a slide to show the lack of attention of mutualism in theoretical textbooks, so I decided to pull some of these books off my shelf to have a visual and some data. The books I owned would, of course, be biased towards including mutualism. But, if the data weren’t too biased, I thought, maybe I’d see a difference between how much attention mutualism receives compared with other species interactions. I haphazardly grabbed 16 and summed the number of pages with the word “mutualism” or synonyms. Here’re the books and data:



Despite expecting a difference, I still found this to be striking. This small, biased sample of texts shows that mutualism is most often mentioned 0 times, and on average it’s mentioned 1 time. This singular mention is always when it’s listed as one of the six types of species interactions. Additionally, if you look at representation of mutualism over time, there seems to be a slight increase in pages and presence of chapters, but nothing that substantially deviates from the figure above.

The number of pages is just one way of assessing how much attention mutualism has received in theoretical texts. We can also look at how authors were discussing mutualism. Allow me to briefly take you through a chronological tour of what the authors have said about mutualism by those that gave at least some space to it:

Christiansen & Fenchel (1973) is a rarity of the ’70s with some text on mutualism:

Mutualism, however, is a special quality of interaction which has rarely been considered from the point of view of theoretical ecology. This is regrettable since a vast number of such relationships, many of which are still incompletely understood, are known from nature.

May (1975, 1st ed. of Theoretical Ecology):

Most contemporary ecology books have chapters, complete with simple mathematical models, on competition and prey-predator. Analogous chapters on mutualism are usually absent. I think the reasons for this are partly historical (Lotka and Volterra studies models for competition and prey-predator, but not for mutualism), and partly because mutualism is a relatively inconspicuous feature in temperate zone ecosystems. Be this as it may, mutualism is a conspicuous and ecologically important factor in most tropical communities, and I hope that the next generation of ecology texts will treat all three types of pairwise interaction between species on a roughly equal footing. . .

Following my admonition in the opening paragraph of this section, I would have liked to include a chapter, along the lines of chapters 6, 7, 8, on mutualism. But I think that neither the theoretical nor empirical aspects of the subject are sufficiently developed to justify this. Many insightful field studies are currently being done, and they should soon provide the basis for such a synthesis

May (1981, 2nd ed. of Theoretical Ecology, with a slight change to the 2nd ed. paragraph from above):

Following my admonition in the opening paragraph of this section, I would have liked to include a chapter, along the lines of chapters 6, 7, 8, on mutualism. But I think that neither the empirical nor theoretical aspects of the subject are yet developed to the point where such a synthetic overview is possible. There are, however, many insightful recent field studies, which shed increasing light on the interplay between the long sweep of evolution and the immediate dynamical effects of populations interactions; it is possible that my laziness is the real reason why such a chapter does not appear in this second edition.

For the record, I deeply appreciate May’s #OverlyHonestMethods here. And to add two notes on subsequent editions: the third edition (May and McLean 2007) only mentions mutualism once (w.r.t. climate change), but the fresh-off-the-press fourth edition edited by McCann and Gellner (2020) has a whole chapter on mutualistic networks (!)

I don’t have a theoretical ecology text from the ’90s with anything about mutualism to quote. May, Roughgarden, and Levin’s Perspectives on Ecological Theory (1989) is almost the ’90s and has chapters on interspecific interactions, but nothing on mutualism. Gotelli’s Primer of Ecology (1995) is another excellent text, but it has no mention of mutualism. Maybe the ’90s were just too angsty to publish then?

Kot (2001) has an entire chapter on mutualism:

Mutualism is an interaction in which species help one another. Mutualism has seldom received the attention of predation and competition. This neglect is quite surprising, given the ubiquity of mutualism.

Vandermeer & Goldberg (2003, 1st ed. has some pages on mutualism in the competition chapter):

That is, as pointed out several times in the past (e.g., Rich and Boucher 1976), mutualism in its various forms is probably the dominant form of interaction in the world yet received the least attention in ecology textbooks. The reason for such a bias eludes ecologists. We follow the traditional orthodoxy of pretending that predation and competition are the dominant forms of interactions, or at least the ones most worthy of the development of theory.

Vandermeer & Goldberg (2013, the 2nd ed. has a chapter on mutualism):

Despite the ubiquitousness of mutualism, no central body of theory of their population dynamics has emerged in the way that it has for predator-prey systems or for competition . . .

To add another line of evidence of underrepresentation of mutualism in theoretical textbooks we can have a look at what is perhaps the most influential monograph series in our field, Princeton Monographs in Population Biology (MPB). Of the > 60 MPBs, only one is focused on mutualism (Bascompte and Jordano’s 2013 Mutualistic Networks). Of the 31 MPBs on my shelf, here is a rough estimate of the number of pages ordered through the series:


I show mutualism (blue) with the one MPB on mutualism (solid) and without (dashed). I don’t think I have to interpret these data because the pattern is clear. Although, I will add that I’m aware of at least 2 MPBs in the works that will have substantial parts on mutualism by M. McPeek and M. Frederickson, so stay tuned.

The pages in theoretical texts, quotes from theoretical texts, and pages in MPB have hopefully convinced you to some extent that mutualism is largely missing from theoretical textbooks. But I also hope that you gained the sense from the quotes that there seems to be a passing of the mutualism buck as you read through the years, where the importance of mutualism will be acknowledged but not given much, if any, attention. And it’s strange because theoretical work on mutualism has been developed and it has been synthesized since the ’70s. Yes, not nearly to the same extent as competition and enemy-victim interactions, but it’s there, and it’s solid work.

I later learned that my observations—or lack of observing mutualism, in this case—were not new. Ecologists have documented this lack of attention for almost 50 years. As early as 1976, Risch and Boucher surveyed 12 textbooks and noted the neglect of mutualism, with 718 pages devoted to interspecific interactions, and 35, roughly 5%, of those were devoted to mutualism. If you’re interested in the history of studies of mutualism, have a look at the first two chapters in the only two general books on mutualism: Mutualism by Bronstein (2015) and The Biology of Mutualism by Boucher (1985) for brief historical accounts.

At this point you’re probably wondering: what is the deal? You may be asking yourself, for instance, if mutualism could not be included in theoretical texts because its ecology is fundamentally different than other species interactions? Is it different? Let’s consider a bit of the ecology of mutualism that might matter for theoretical models:

  • Some mutualisms occur between organisms with large differences in generation times or body sizes: this is true of other species interactions
  • Mutualism sometimes involves species beyond simplified two-species motifs: this is also true of other species interactions
  • Some mutualisms are behaviorally mediated with no direct contact: yup, this happens in other species interactions, too
  • In some mutualisms the effects on fitness is delayed: uh-huh, this is also true of other species interactions
  • Mutualism has costs and benefit: definitely true of other species interactions
  • Mutualism is dependent on ecological context: which is, yet again, true of other species interactions
  • Mutualistic interactions are facultative or obligate: TOOSI (True Of Other Species Interactions)
  • Mutualistic interactions span specialized and generalized: TOOSI
  • Some mutualistic interactions are consumer-resource interactions: #TOOSI
  • And so on

It seems like maybe that mutualism might not be that different after all? . . . If we are willing to view other species interactions as simplified spherical cows and massless horses in our simple theoretical models, then we ought to be consistent by also allowing the mutualistic llamas to be frictionless in vacuums and have other simplified properties for the sake of educating readers of textbooks and theoretical development. Also, thank you for bearing through my stretching the spherical-cow metaphor across the ungulate and physics axes 🙂

Another reason that mutualism might not be included in theoretical texts is because of the spectre of unbounded growth. The late Robert May famously described mutualism as “an orgy of mutual benefaction.” This comes from the simple two-species Lotka-Volterra model of mutualism developed by Guase and Witt in the ’30s by switching the sign of the competition model from –  to +. In this model, if the mutualistic benefit is greater than intraspecific competition, then the populations grow exponentially without bound. This seems to be the central focus of this model—but perhaps it shouldn’t be. Unbounded growth shouldn’t be the central focus of the Lotka-Volterra mutualism model because it is a theoretical inconvenience and a consequence of the model structure; unbounded growth is not a feature of real populations. We should therefore not ignore mutualism because the model we chose to use produces silly results. Instead we should focus on the facts like that even in the overly-simplified, general Lotka-Volterra mutualism model, we find that mutualism increases species’ abundances at equilibrium(!) and increases population growth rates(!). It even seems like showing how mutualistic interactions are kept from unbounded growth would be a good transition in textbooks between 2 to 3-n species models or as a way to introduce nonlinear functions or numerical solutions.

Mutualism, as the quoted authors above and many others contend, is ubiquitous and incredibly important for communities and ecosystems. I don’t have the space in this blog to further elaborate on the reasons why mutualism receives less attention, but again see Boucher (1985) and Bronstein (2015) for their historical treatments. In the end, to channel May, it is possible that my laziness is the real reason I why a further elaboration does not appear in this post.

For those of you looking for material on mutualism to add to your textbooks, there is a ton of great work out there, but here’re a few foundational references and several references to newer, exciting work in mutualism theory (of simple, low-dimensional systems, not the exciting explosion of literature on mutualistic networks):

A few classics:

  1. Vandermeer, J.H. and Boucher, D.H.,1978, Varieties of mutualistic interaction in population models. Journal of Theoretical Biology, 74(4), pp.549-558.

Introduces facultative and obligate interactions into the Lotka-Volterra mutualism model

  1. Wolin, C.L. and Lawlor, L.R., 1984. Models of facultative mutualism: density effects. The American Naturalist, 124(6), pp.843-862.

Considers the effects of intraspecific density in mutualistic interactions and explicit nonlinear functions (a personal favorite)

  1. Wright, D.H., 1989. A simple, stable model of mutualism incorporating handling time. The American Naturalist, 134(4), pp.664-667.
  • Adapts Holling’s Type II functional response to mutualism

Just several (limited to 6) of many recent (last 5 years) works that I find exciting:

  1. Johnson, C.A. & Bronstein, J.L., 2019. Coexistence and competitive exclusion in mutualism. Ecology, 100(6), p.e02708.

Develops analogous R* rule for coexistence of mutualism

  1. Wu, F., Lopatkin, A.J., Needs, D.A., Lee, C.T., Mukherjee, S. & You, L., 2019. A unifying framework for interpreting and predicting mutualistic systems. Nature communications, 10(1), pp.1-10.

Derives and evaluates a simple rule for understanding mutualistic interactions

  1. Revilla, T.A., 2015. Numerical responses in resource-based mutualisms: a time scale approach. Journal of Theoretical Biology, 378, pp.39-46.

Explicit look at consumer-resource nature of mutualistic interactions and ecological meanings of saturating function parameters

  1. Hoek, T.A., Axelrod, K., Biancalani, T., Yurtsev, E.A., Liu, J. & Gore, J., 2016. Resource availability modulates the cooperative and competitive nature of a microbial cross-feeding mutualism. PLoS biology, 14(8), p.e1002540.

A simple microbial cross-feeding mutualism experiment supported with a simple model

  1. Hale, K.R.S., Maes, D.P., & Valdovinos, F.S., 2020, The ecological theory of mutualism: Models generalizing across different mechanisms, Contributed Poster, Ecological Society of America’s Annual Meeting

Very new formulation of models specific to protection, nutritional, and dispersal (pollen and seed) mutualisms

  1. Nakazawa, T., 2020. A perspective on stage‐structured mutualism and its community consequences. Oikos, 129(3), pp.297-310.

Develops general theoretical framework for incorporating stage-structure and developing an ontogenetic perspective of mutualism

I also want to give a shout out to all those that have included theory of simple mutualisms (not comprehensive); e.g., DeAngelis et al. (Positive feedback in natural systems, 1986), Holland (in Mutualism, edited by Bronstein, 2015), Kot (Elements of mathematical ecology, 2001), Morin (Community ecology, 2011), Stadler and Dixon (Mutualism: ants and their insect partners, 2008), Vandermeer and Goldberg (Population ecology: first principles, 2013), and Wolin (in The biology of mutualism, edited by Boucher, 1985).

There has been so much outstanding work on theoretical aspects of mutualism ecology and evolution over the last four decades, and I’m sorry I cannot include all of it here! Perhaps you can add your favorites in the comments and add to this blog so it can be used as a resource.

Thanks to J. Bronstein and J. Dittel for comments on an earlier draft of this post.

Thank you for reading and I hope you enjoyed it!

40 thoughts on “Passing the mutualism buck: why have theoretical textbooks largely ignored mutualism?

  1. That’s a great post Chris, and kudos to Jeremy for giving you the space to write it. You’re correct of course, mutualism has been grossly neglected, and not just in the theoretical texts, but also in the general ones.

    It’s hard to fathom why this is the case, but there have been a few hypotheses mooted. I forget where I read it, possibly in the Boucher volume, but there’s a long-standing suggestion that the relative lack of work on mutualism (both theoretical and empirical) has both political and sexist roots. The political argument has it that capitalism “red in tooth and claw” is more likely to result in work showing that species negatively exploit each other. The gender argument holds that men (who historically dominated ecology) were more likely to be drawn to “macho” fields such as studying large predators.

    I’m not suggesting either is a correct explanation. But anyone who thinks the political argument might be far fetched should note that there’s a large historical body of (mostly untranslated) research literature on mutualism from the USSR. And before dismissing the gender argument, take a look at this written account of the toxic masculinity of shark ecology:

    Another possible explanation is a silo mentality in ecologists working on mutualisms: not many cast their nets wider than their chosen type of study system, so pollination ecologists and mycorrhizae specialists rarely interact, for instance, even though they could teach each other a lot. In some of my work I’ve tried to broaden the boundaries and show the commonalities between mutualisms (notably in my “biological barter” book chapter – reference below) but getting to grips with even the basic natural history of such a diverse set of interactions is hard work. But I think it’s worth it and could provide insights into how nature really works.

    Ollerton, J. (2006) “Biological Barter”: patterns of specialization compared across different mutualisms. Pp. 411—435 in: Waser, N.M. & Ollerton, J. (eds.) Plant-Pollinator Interactions: from Specialization to Generalization. University of Chicago Press, Chicago, USA

    • Thanks so much Jeff! Boucher did lay out those hypotheses you mentioned. Bronstein (2015) summarizes the hypotheses in Ch. 1 as:
      – Culture (from Keddy 1989): since it’s not given attention, it receives less attention
      – Political connotation (Boucher 1985, Margulis 1990): mutualism had been touted by socialists and anarchists, which made western scientists averse
      – Gender (Margulis 1990): males are more aggressive than females, it was argued, so the patriarchal scientific enterprise focused on more aggressive interactions, like competition and predation
      – Taxonomic (Keddy 1989): there are taxonomic biases in what we study (e.g., affinities for hairy, feathered, and cute things), and mutualism is putatively less a part of their ecology
      – Geographic (May 1982): mutualism in the temperate zones, where most western science is conducted, is relatively inconspicuous
      – Theoretical (May 1982): unbounded growth as mentioned in the post
      – Excitement (Keddy 1989): watching something kill something, or a a parasitoid pupate, or a horesehair worm or bot fly emerge from a host is just hotter material than a bee visiting a flower or an elephant defecating seeds.

      I would add another hypothesis for now:
      – Experimental feasibility: other interactions are more easily experimented on in controlled settings, like petri dishes, bottles, greenhouses, and mesocosms. If we had early population experiments, perhaps that would have fed into population-level theory earlier. Also, as I was reading some of “The Dialectical Biologists” last night, this paragraph resonated with me:
      “The great success of Cartesian method [reductionism] and the Cartesian view of nature is in part a result of a historical path of least resistance. Those problems that yield to the attack are pursued most vigorously, precisely because the method works there. Other problems and other phenomena are left behind, walled off from understanding by the commitment to Cartesianism. The harder problems are not tackled, if for no other reason than that brilliant scientific careers are not built on persistent failure. So the problems of understanding embryonic and psychic development and the structure and function of the central nervous system remain in much the same unsatisfactory state they were in fifty years ago, while molecular biologists go from triumph to triumph in describing and manipulating genes.” (An old passage, but seemingly relevant.)

      These are just hypotheses, some of which are more viable than others. I think the silo idea is interesting. I wholeheartedly agree about the tendencies of some mutualist groups not broadening their perspective, but perhaps it is because there hasn’t been a theoretical base that unites us all?

      I had that book on loan indefinitely from the library in grad school—I need to look at it again! Thanks for the reference and sorry I missed it 🙂

      • Gotta say, I’m fairly skeptical of the Margulis hypothesis that mutualism is understudied by ecological theoreticians who live in capitalist countries because of purportedly anti-competitive implications. I mean, there are a number of prominent evolutionary thinkers who didn’t have much to say about mutualism despite being avowed Marxists/communists (JBS Haldane, John Maynard Smith, Stephen Jay Gould, Richard Lewontin). Conversely, Darwin himself was no communist, but was really into plant-pollinator mutualisms and their evolution by natural selection, emphasizing that mutually-beneficial interspecific relationships emerge from competition (in a broad sense) within species. Lots of evolutionary biologists followed in Darwin’s footsteps, right on up to the present day. Think for instance of all the recent interest in theoretical models of resource exchange mutualisms, inspired by capitalist economics models of gains from trade. And think of how Darwin’s theory of evolution was interpreted by some as justifying capitalism, and by others as justifying communism. So I don’t think there’s any simple straightforward story to be told about the neglect of mutualism in theoretical ecology for political reasons.

      • Was just going to make a political argument referencing Dialectical Biologist, but yay you both got there right away! I’m thinking a lot about how “capitalism red in tooth and claw” is pervasive through all of biology (and writing at the moment about it in the field of behavioral ecology), and thinking about how certain organisms/questions become much less tackle-able from within that capitalist paradigm, and some things–like mutualism here, and in my case, tent caterpillars–represent these really clarifying examples of paradigm-fueled un-tackle-ability.

      • “certain organisms/questions become much less tackle-able from within that capitalist paradigm, and some things–like mutualism here, and in my case, tent caterpillars–represent these really clarifying examples of paradigm-fueled un-tackle-ability.”

        But are they untackleable, Ambika? Again, in evolutionary biology I don’t feel like mutualism has been untackled or untackleable, from Darwin onward. In theoretical ecology–especially theoretical population biology–I agree with Chris that mutualism has been neglected, at least relative to competition and predation. But of the hypothesized reasons for that comparative neglect, my money’s on a combination of “if you stick positive competition coefficients in a Lotka-Volterra model, it tends to predict explosive growth to infinite abundance” and “it’s been neglected in the past, so it keeps getting neglected”. Rather than on “capitalism”. I just am struggling to square the “capitalism” hypothesis with the historical “data” from evolutionary biology. Am I way off base on the history here?

      • @ Jeremy–Maybe “tackle-able” was the wrong (made up!) word…but I do think it’s worth asking why something gets neglected over and over again beyond simply saying, well it was neglected in the past and so we continue to do so. Because we do value novelty too, which would argue for the opposite effect, right? And you can think of mutualisms from an individual self-interest perspective, of course, in the way that squares nicely with a Darwinian approach and with capitalism, but I have a strong sense that the science of mutualism (and tent caterpillars!) would look very different from a perspective that wasn’t centered on the shared premises of capitalism and individual-based narratives of natural selection. Anyway, this will be the subject of the talk I give at Calgary in the spring, so we can argue more then too, by which time my thoughts will be better formed 🙂

      • Yes, looking forward to your talk!

        “Because we do value novelty too, which would argue for the opposite effect, right? ”

        Yes. Which kind of highlights why I’m reflexively suspicious of simple blanket stories about why scientific topic X is little-studied, or why hypothesis P was proposed to explain phenomenon Q but hypothesis R wasn’t, or etc. It’s not that I think scientists’ individual or collective decisions about what to study, what hypotheses to propose, etc., are somehow decoupled from the broader milieu. It’s just that I think those connections are often very complicated and tangled, and that they vary a lot from one individual scientist to the next, and from one scientific topic or field to the next. The choices of individual scientists, and the collective choices of entire scientific fields, are shaped by *lots* of interacting factors, the balance between which seems difficult to sort out and varies a *lot* from one case to the next. So, it’s like ecology, pretty much. 🙂

      • I find the capitalism argument incredibly compelling. Any human idea, scientific or otherwise, needs to be considered within its social and cultural context. While conclusions about a direct causal relationship between capitalism and an ecological focus on competition are noisy, they cannot be dismissed out of hand. Social theory reminds us that we are all born into a culture and this culture shapes thinking: the snap second decisions we make about what ideas we think sounds “interesting,” the snap second decisions we make about WHO we think sounds “smart,” decisions about what piece of the story to investigate further. These decisions are all heavily influenced by the culture we swim in. Are there outliers? People who buck the trend and push for new ways of thinking? Definitely. But the fact that these new paradigms don’t catch hold is further evidence that the community of scientists is not “compelled” by these alternative visions. What makes the community of scientists compelled or not? Well that is heavily influenced by culture. Anyway, I also enthusiastically recommend reading more broadly about the role socialization plays in affecting how we think. A GREAT intro to this subject for ecologists is to go back and read (or re-read) Ishmael. 🙂

    • Thanks Chris for the thoughtful post, and Jeff for the thoughtful comment. Jeff- how can I get into the USSR literature on mutualism? Happy to start translating, I just don’t even know where to start!

      I have had several conversations where people suggest less capitalists countries have different theories of ecology that are less rooted in competition. In our scientific discourse, we are constantly asking “but what prevents cheating the mutualism?” rather than challenging, “what is preventing cooperation in this system?” Even Marx argued that capitalism is much bigger than an economic system, it pervades all aspects of culture. Its hard to imagine it doesn’t affect how we think and do science.

      • Hi Colin – I strongly suspect that the early Soviet literature has never been digitised so one would need to find a library, or a colleague with an access to a library, that holds Soviet literature from the early/mid 20th century. Some judicious googling might throw up a few clues.

        Interesting observation regarding preventing cheating v cooperation. If you look at that book chapter I referred to, I point out that there are some, perhaps many, mutualisms that are inherently stable in the sense that cheaters can’t evolve. The system is uncheatable because as as soon as a partner cheats, the system fails to function. Since then I’ve done a bit of work on the anemonefish-sea anemone relationship (references below) and this seems to be a good example of an uncheatable system. It’s one of the few mutualisms where two animals are actively providing one another with physical protection and if the anemone fails to protect the fish, the fish will move on or be predated, and the anemone will lose its aggressive protector and get eaten by butterfly fish. Conversely if the anemonefish fails to protect the anemone, again the anemone will be eaten, and the anemonefish will be predated. As far as we know there are no cheating species of either anemonefish nor anemones.

        Just to pick up on a comment made above (I think by Chris) about mutualism not having any famous experiments such as hares/paramecia/etc. That’s true, though it’s worth pointing out that one of Gause’s foundational experiments (if I recall it correctly) showed stable coexistence between Paramecium bursaria and P. caudatum in part because P. bursaria hosts symbiotic algae that provide it with energy even when it’s competing for food. So a mutualism is fundamental to this classic system, though I don’t know enough about Gause’s work to say whether he explicitly discussed that connection. Perhaps Jeremy can comment?


        Ollerton, J., McCollin, D., Fautin, D.G & Allen, G.R. (2007) Finding NEMO – nestedness engendered by mutualistic organisation in anemonefish and their hosts. Proceedings of the Royal Society series B 274: 591-598

        Ricciardi, F., Boyer, M. & Ollerton, J. (2010) Assemblage and interaction structure of the anemonefish-anemone mutualism across the Manado region of Sulawesi, Indonesia. Environmental Biology of Fishes 87: 333-347

  2. Wow, amazing post! Thank you very much for sharing your ideas and findings. I’ve had a very similar experience myself.

    Mutualism has always been my major interest in science since undergrad times. Sadly, this topic was indeed virtually absent in most textbooks, monographs, and reviews I consumed during my formative years. But it was not absent in studies carried out here in South America! Many scientists from the periphery have always been deeply involved in studying pollination and seed dispersal, among other positive interactions. Unfortunately, as usual, voices from the South are ignored and our findings are seldom added to big theories. This started to change substantially only in the 2000s, when peripheral ecology finally reached a momentum in the mainstream literature.

    And I agree with you: mutualisms are not so different from antagonisms in many theoretical and empirical aspects. Current evidence shows that many species traditionally considered textbook examples of mutualists or antagonists are dual players in fact. Furthermore, several relationships between species are also dual, changing from positive to negative and back constantly, depending of intrinsic and extrinsic conditions. Interactions are very taoistic and nature does not fit overly simplified boxes.

    Consequently, transcending the illusion of duality should be the next step in the development of the body of knowledge about species interactions.

    • “urrent evidence shows that many species traditionally considered textbook examples of mutualists or antagonists are dual players in fact. Furthermore, several relationships between species are also dual, changing from positive to negative and back constantly, depending of intrinsic and extrinsic conditions. ”

      I feel like there’s been a fair bit of theoretical (and empirical) attention to that aspect of mutualisms, but in evolutionary biology rather than ecology? Evolution of mutualism from parasitism, etc.

      • There’s plenty of ecological, even population dynamic papers on mutualism. Nat (J. Nathaniel) Holland has several. I have one. Roughgarden has one. None of them have the degree of generality of a Lotka Volterra or Rosenzweig & MacArthur model though.

      • Actually, I would risk saying that there are much more papers on mutualism in the ecological literature than in the evolutionary literature. But I’m biased, as I read much more ecology than evolution. Theoretical ecological papers on mutualism date back to the sixties, at least. Pioneers like the Sazima couple paved the road we follow nowadays.

    • Strong agree with your comment! Especially “Unfortunately, as usual, voices from the South are ignored and our findings are seldom added to big theories.” In 1994 Bronstein’s “Our Current Understanding of Mutualism” (Quarterly Review of Bio.) found, compared to other interactions, mutualism was represented in the literature (10 journals from ’86–’90): about 1/4 of interspecific interaction studies. So, it seems like it was being studied widely geographically and present in journals and just not adopted into the mainstream/texts.

      I’m also excited to see where variation in interaction direction leads us—it’s a really exciting line of work that’s being done right now!

  3. Nice review! I also believe John N Thompson’s books are great sources for general info on mutualism. Also, the new theoretical ecology book that just came out, has a whole chapter on mutualism!

  4. I also forgot to mention, the new book titled “unsolved problems in ecology” has a chapter by Egbert Giles Leigh Jr. On the ” neglected problems in ecology: Interdependence and Mutualism” . It summarizes the neglect of mutuliams in ecology and why biologists should read “the wealth of nations by Adam Smith” in order to fully appreciate mutualism .

    • “why biologists should read “the wealth of nations by Adam Smith” in order to fully appreciate mutualism”

      There’s another data point arguing against the hypothesis that “capitalism” is the primary reason for the neglect of mutualism in theoretical ecology!

      • Adam Smith hinted at the idea of trade due to comparative advantage but Ricardo developed it much more fully and there is quite a bit of literature on the linkages between Ricardo’s theory and mutualism. Indeed Ricardo may be the only time I’ve cited an economics book (non-game-theory related) in an ecology paper. (oops just looked, I cited Smith in the same paper).

  5. Hi,

    Very interesting post! One question that comes to mind is this. Given that mutualism has been relatively ignored/dodged in the theoretical ecology literature, but non-theoretical work has happened on it (the field studies that May refers to, for example), has the development of this field been different compared to that of other fields of species interactions where theoretical work has been relatively prominent, for example coexistence, predation and competition? One caveat is that I suppose it might be difficult to conclude that any differences in development are due to the differing presence of theoretical literature, because other variables may also co-vary.

    I can’t immediately think of any clear differences that one might expect in the field of mutualism compared to fields of other species interaction – one vague idea is that, from whatever I’ve read so far, generally theoretical work in ecology is inspired in many of its ideas by physics and maths, and often provides a general, abstract framework that focuses on dynamics and equlibria, while a lot of field work is built on natural history observations and explaining specific patterns seen in nature. This is loosely analogous to top-down vs bottom-up models of research, and perhaps in the field of mutualism there might be much more of the latter than the former compared to other fields of species interactions.

    It might be quite depressing if there are NO differences, though – because that might then point to the lack of communication between theoretical and empirical work in ecology.


    • Thank you so much!

      I think this is a really good question! I cannot say that I am versed as well in those other areas of theory to be confident in a response. I will make note of a couple of things, however:

      First, you are completely right about broad development of mutualism has been different. A major difference, in my opinion, is the population-level studies for mutualism are comparatively rare. In my reply to Jeff Ollerton above I note that I see this as a hypothesis why population-level theory may not have made it into textbooks. I have a paper that I have presented at meetings a couple of times that I will have out soon that synthesizes certain population-level studies of mutualism. Those are rare. Descriptive, behavioral, community studies all seem to be considerably more common. I don’t think that mutualism has its famous controlled population lynx-hare/yeast/paramecium/mites experiments yet. There is good mutualism work focused on populations of engineered microbes (e.g., Shou et al. 2007 PNAS, Yurtsev et al. 2016 PNAS), but I don’t know if these are or will be foundational population studies of mutualism.

      Second, I like your comparison of top-down and bottom-up to analogy and observation to make theoretical inference. I once had a physicist who was considerably smarter than me ask me about mutualism. They seemed to only want to know about dynamics (specifically oscillations) in mutualistic systems, which I attributed to their training. If mutualistic species oscillate in nature did not seem to be of interest to them, which made discussion a bit difficult. I think both approaches are needed and complimentary. I effectively knew no theory before my postdoc and my approach has been to try to add observed/ecologically-based terms into theory since the high-level stuff was/is not accessible to me. So, that’s my bias in all of this.

      I wonder how one would go about analyzing bodies of theory to answer your question. Now I’m curious!

  6. I think a key point here is that the original post is talking about theoretical ecology. Although the case has been made that mutualisms are ignored more broadly, I think most modern general ecology textbooks give at least a full chapter to mutualisms which is not so different to the treatments for competition or predation.

    So I think this has to at least raise a question of whether the problem is with theoretical ecology, not with mutualism and its treatment in ecology.

    I’m going to make a controversial statement. The primary contribution of theoretical ecology has centered on themes and variations of the effects of negative density dependence (and to a much lesser degree negative frequency dependence) as the central regulatory mechanism and driver of dynamics. This makes it inherently well suited for studying negative interactions but poorly suited for studying positive interactions. Hence the logistic equation, Lotka-Volterra and Rosenzweig MacArthur.

    I presume we’re past the density dependence wars and that most people recognize that there is density dependence in the world but also other forces acting as well (I have to assume Andrewartha and Birch would be rather pleased to see the modern emphasis on climate change impacts on populations and distributions of species). But theoretical ecology is really mostly only equipped to deal with those parts of ecology involving negative density dependence.

    Now any species in a mutualism experiences negative density dependence (or it would show exponential growth), but the density dependence comes from factors OUTSIDE the mutualism (e.g if a plant receives nitrogen from a mutualism it is limited by space). So a simple mutalism model doesn’t have negative density dependence. And thus theoretical ecology is ill-equpped to tell us anything interesting about mutualisms.

    A closely related point is that theoretical ecology loves extremely general phenomenological models like Lotka-Volterra (that is what we really mean when we say theoretical ecology ignores mutualisms because as I cited in a comment above there are actually dozens of mathematical models of mutualisms). And it is why theoretical ecology does negative density dependence well – assume 1/N dN/dt is a negative function of N. But the central feature of mutualisms (an exchange of goods or in economics exploiting comparative advantage) is not that easily modelled as a sweeping phenomenological mathematical function (at least that has been invented to date). Or maybe its more the case that its just not that interesting to model it with sweeping generality. Hoeksema and Schwartz have a paper pointing out that the math from economics of comparative advantage applies generally. It just hasn’t been picked up very much.

    TLDR summary – there is plenty of attention to mutualism in ecology and even a very general overarching conceptual model (comparative advantage trade of goods). There are also plenty of more narrow, system-specific detailed mathematical models of mutualisms. So mutualism are in no way ignored. Its just that theoretical ecology has nothing to add to mutualisms in the way that theoretical ecology judges good (sweeping general models centered around negative density dependence). So theoretical ecology will always ignore mutualisms unless and until theoretical ecology itself changes.

    • Thanks for your response and great points Brian! I was actually at UMaine giving a seminar (in-person, if we can remember those days) in early February of this year and missed the chance to talk with you about some of these ideas!

      I agree with your claim that most modern general ecology textbooks have chapters on mutualism. That being said, as someone who recently began teaching and was recently looking for ecology textbooks, there were absolutely none without competition and none without predator-prey. I should have tried to dig up data on general ecology textbooks too, but maybe for the next post 😉

      One thing that is a little more subtle and nuanced that I didn’t include but is important is the way that we talk about mutualism and not just the presence and absence of chapters or pages. I won’t go into detail here, but I’d argue the way that we talk about mutualism is different compared with other interactions, too. For instance, concepts of symbiosis or context dependency, are often bundled with mutualism and *sometimes* take up a disproportionate amount of space. Symbiosis is relevant for other interactions, too. Context dependency is a feature of all species interactions, too. A great read is Chamberlain et al. (2014, Eco. Lett.) who showed that predation, competition, and mutualism were not different in their degree of context dependency. I’m not saying either symbiosis or context dependency is not important whatsoever and I think that people who study mutualism have made important contributions to those ideas, but by bundling mutualism with these other ideas sometimes mutualistic spaces look different than other interactions.

      I need to think about “The primary contribution of theoretical ecology has centered on themes and variations of the effects of negative density dependence (and to a much lesser degree negative frequency dependence) as the central regulatory mechanism and driver of dynamics.” I don’t think that I disagree, but I will state what I think we agree on, which is that what we focus to study is not always the full or even most important/explanatory feature of nature.

      How much we abstract ecological systems is often fairly subjective. We can choose to make any model as complex as we want, usually depending on our analytical capabilities and the purpose of our modeling endeavor (fitting data, adding biological realism, exploring dynamical behavior). In theoretical textbooks it seems like simplicity and elegance are the priorities because those are easy to teach and learn from, communicate, and have great heuristic value. They also are created to capture and generate qualitatively-important features and behaviors of real populations, the kinds that MacArthur and Levins favored. Species engaged in mutualism are affected by other species or resources in a multitude of ways, just like with other interactions. Abstracting to 2 species and making the distinction between intrinsic and extrinsic negative density dependence seems a bit arbitrary. Can mutualism not be qualitatively described and inform without resources or other species like we do with other species interactions? I think so, or at least as much as other interactions.

      I also want to agree and emphasize your comment in two of your replies: there is a great body of theoretical work exists in the literature, and I only listed a few there at the end. Holland’s is important and is the foundation for (all?) dynamic mutualistic network theory since 2006. These theoretical papers just don’t seem to have made their way to theoretical texts. I should have emphasized that more, but I feel like I already have so many words! There are really too many things to talk about!

      • Hi Chris,

        I was really sorry to miss you in February and hope when this is all over we can connect – we’re only over an hour apart.

        I really like your point about how mutualisms are treated differently. I totally agree with your point about how context dependence is emphasized much more for mutualisms (and facillitation) even though it is not at all specific to mutualisms. I would add that much more effort goes into taxonomy of mutualisms. We have ideas like food-food vs food-transport or food-service mutualisms and then we do a nature show tour through different mutualisms. Competition and predation are just as diverse. There have been a few attempts to make taxonomies of competition but nothing more than interference vs exploitation has really stuck (and is not strongly emphasized). And in +/- interactions we don’t even attempt to lump predation, disease, herbivory, parasitism into a unifed concept – the taxonomy is too strong.

        As to your point about distinction between intrinsic and extrinsic density dependence between arbitrary and possibly uninteresting. I guess my thought is it depends on the goal. The goal of Lotka-Volterra and Rosenzweig-MacArthur is to identify equilibrium states. There is nothing in the intrinsic features of a mutualism that create an equilibrium. So if the goal is an equilibrium, then you have to invoke extrinsic factors. I would agree though that this is a problem with the goal. Modelling of mutualisms should reject identifying equilibria and focus on intrinsic complexities like cheating, specialist vs generalist, etc (this echoes Dave Armitages point below).

        I’m curious if you’re happy with comparative advantage as an overarching framing of mutualism even if it hasn’t led to a general strategic model that makes theoretical ecologists happy?

        (Really great post by the way!).

      • Thanks so much Brian! Yes, I’d love to connect when this is over.

        Good points about taxonomy of interactions. I often think about competition, but the taxonomy of enemy-victim interaction is so strong that I often forget they are the same!

        If the goal to identify equilibrium states, ignoring whether or not there is a problem with that goal, then I don’t think mutualism is so different than other interactions. For instance, with the ordinary linear interaction terms Vandermeer and Boucher identify equilibrium of states, depending if each species is obligate or facultative and the strength of those interactions. Some interior equilibria are stable and other are unstable. Another example would be the presence of 2 stable states: one extinct and one positive on the other side of an allee threshold. Off the top of my head the earliest mention of this was May in Theoretical Ecology. This positive density dependent feature of mutualism has shown up fairly often through the years (e.g., a relatively recent paper off the top of my head is Johnson and Amarasekare, 2013, JTB). So, I think the states are there, but like you mention, I think rejecting identifying equilibria as the only important goal is probably a good thing.

        I think comparative advantage is an enlightening and useful framework. As Dave also points out, I think there will undoubtedly be a lot to gain from looking at the intersection or synthesizing different frameworks. This is something we should talk about post-pandemic!

  7. Nice post!
    I did not see this explanation, related to taxonomy. As ecologists we tend to have our favored organisms (e.g. fish, or algae). However mutualisms happen where the aspect that provides benefit to organism A is cheap to organism B, and vice versa. Organisms that are more closely related are less likely to differ in the way and more likely competing for the same things. So if we focus on our favorite organisms, we tend to miss mutualisms (unless we love flowers).

    Second point I would make is that in terms of direct interactions, neutralism is probably the most common (0/0), followed by amensalism and commensalism, and these mostly get even less theoretical attention (except for concepts like connectivity perhaps) (

    I also published a model years ago with mutualism that showed that mutualisms embedded in a competitive matrix gave pairs and advantage (mostly ignored … ah well)

    To be honest, as a grad student/ postdoc/ early faculty member I was really gung-ho on mutualism and how it played into theoretical community ecology, but that was not popular, I never got much traction with established theoretical ecologists, and in the end I moved on to other things…

    • Thanks so much!

      Good point Re: taxonomy! In response to one of the comments one of the hypotheses was taxonomy, but not as it related to distance.

      Good point about 0-interactions! In a new Annual Review just a few weeks old, Mathis and Bronstein review and call for more research into commensalism ( I think these interactions will be seeing much more prominence in the future; especially, as they argue, because the magnitude of interactions is often dynamic and often near 0. I have likened the distributions of interactions in communities to that of mutations: before we measured them we ignored the idea that most were neutral and debated if more were fitness increasing or decreasing. If we were to look at the distributions of pairwise interaction effects, like you, I suspect they’d mostly be neutral, with more 0/+ and 0/-, and fewer +/+, +/-, and -/-. Maybe METE could give us an a priori prediction of what this distribution would look like here?

      These papers look great—thank you for referencing them! I’m eager to have a look over them; especially the mutualism paper!

      • There are relatively few studies that try to census (or randomly sample) lots of interspecific interaction strengths in nature. But yes, the very broad-brush generalization seems to be that the distributions are skewed–most interspecific interactions are pretty weak, only a small minority are very strong. So yes, ~0/~0, ~0/+, and ~0/- should outnumber +/+, +/-, and -/-. The consequences of that for population and community dynamics could be interesting, and they’ve received some theoretical attention (for instance from Kevin McCann), but very little empirical attention. The sorts of experiments you’d want to do are pretty technically challenging, even in the microcosm system I work in, never mind in a field system.

      • Chris, Interesting point about using METE to look at network structure. Rich Williams (2009) worked out for bi-layer networks the distribution of edges across nodes using MaxEnt and it works pretty well, but I think the more tantalizing problems are a. distributions of linkage-types across nodes (as you said), b. distribution of flow rates, not just presences of links, c. extension to networks more complex than bi-layer.

        What I find especially fascinating is the interplay, within a network, of mutualism and competition. Acting together they allow inference of a sweet spot where the competitor doesn’t over-compete and hurt her mutualist partner or unnecessarily under-compete. Ann Kinzig and I explored the optima that result nearly 3 decades ago for simplified biogeochemical networks and reached some fairly realistic conclusions:

        Brian, I wonder whether the simple models we used could have application to economic systems, where there is a similar interplay of mutualism and competition.

      • Thanks John. I’ve always been curious if METE had the ability to predict the distributions of interactions in this way. I only have a cursory understanding of METE from a few papers and a few chapters out of your book, but I’ve looked for something along these lines and not seen anything. As Jeremy noted above, it would be empirically challenging (or, to me, maybe impossible) to estimate the distribution of interactions. So maybe we have to rely on theoretical methods? But I also wonder if we can look at the distributions of signed edges of other complex systems that are more easily studied through analogy? I am imaging, for instance, the distribution of up- and downreglation in gene regulatory networks? Maybe even social networks with friends and enemies (as I understand the terminology)? But some that would be relatively easy to find data on, like the internet or airports, aren’t signed networks as far as I understand.

        Also, that study of yours is great! Your link was directed to the Berkeley library, so here’s a link to the Am. Nat. paper:

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