Can stealing from your neighbor be a mutualism?


Imagine that your neighbor sometimes goes into your house and takes some food out of your fridge. Sometimes you catch her, but you don’t get violent about it, you just push her out and tell her to not come back. But she keeps sneaking in.

Imagine that you’re also stealing food from your neighbors. Imagine that everybody in your neighborhood is stealing food from one another.

This is pretty much what happens with thieving ants (Ectatomma ruidum). These ants act like bouncers and kick out their neighbors when they catch thieves. They don’t get violent like you would expect from most ants. But they do put in effort to detect and boot out thieves.

Does this sound weird and not make that much sense? That’s what I think, and that’s why I’m working to figure it out.

In a paper from my lab that was just published in the journal Biotropica, we asked the questions: Does the vigilance against thieves respond to the intensity of thievery? In a world in which these ants didn’t steal from one another, thievery existed, would everybody be better off or worse off?

If thievery was some kind of mutualism or reciprocal altruism, then you’d expect the loss of thievery to harm productivity at the colony level. If thievery is truly exploitative and parasitic, then stopping thievery would boost productivity throughout the system.

So, we created that world-of-no-thievery, by removing all of the thieves, and measured productivity by collecting colonies at the end of the experiment. And we measured how the removal of thieves affected how sensitive colonies are to interlopers.

Here is the paper itself:

Jandt, Jennifer M., Elizabeth M. Hunt. 2015. Intraspecific Food-Robbing and Neighborhood Competition: Consequences for Anti-Robber Vigilance and Colony Productivity. Biotropica. DOI: 10.1111/btp.12234

So what did we find? Thievery is not a mutualism, and when you remove the thieves from the system, everybody is better off!

Colonies collect their own food, but they also are taking it from their neighbors. When the removal of food from the neighbors stops, then everybody gets more successful. In game theoretical terms, the cost of defecting and stealing — and being stolen from, is less worse than the sucker’s payoff of not stealing at all.

How this project happened in the context of an undergraduate institution:

My lab has been working on this system for a field seasons. (Here is the post about our first paper on the topic). This project was a collaboration among myself, Jenny Jandt, and Beth Hunt. Beth was a student from my university who conducted this project as a part of our International Research For Experiences for Students program. Her primary mentor for this project was Jenny, who had the experience and availability to mentor Beth throughout the field season.

You’ll notice in the methods that the project was conducted in the summer of 2011. After the field season ended, we worked on the paper on and off for a while, and somewhere in there, drove to Arizona to work with Jenny for a long weekend to work on this paper (and also another one.) Getting the paper out four years later is par for the course I’m playing on. But if you happen to be in Hawaii this week for the Tropical Biology meeting, you can catch the next installation!

This work was supported by the U.S. National Science Foundation (OISE-0854259 & OISE-1130156).

13 thoughts on “Can stealing from your neighbor be a mutualism?

  1. Terry, any reason you opted for Biotropica over a more behavior-orientated journal? I haven’t yet been able to access the paper but the topic as you pitch it strikes me (as a behavioural ecologist) as a question that has been dealt with frequently in such journals.

    • Jesse, the paper was written (mostly) by Jenny, who is a behavioral person, whereas I’m an ecological person. While its pitched as a primarily behavioral question, I think the ecological piece is central and what I’m into. I’m kinda surprised that this system isn’t more widely known as an amazing thing, even though its biology was well described in Animal Behaviour by Mike Breed a couple decades ago. So I want people outside the behavioral world to know about it. That’s also why I chose this system for my talk at ATBC this week.

      I also am an evangelist for tropical biology, and as a member of the Biotropica editorial board, I think I should make a point to send some of my better work to the journal. I imagine this will steadily pick up citations over the years, which isn’t bad for the journal.

      Also, Biotropica publishes other behavioral work too – its covers all kinds of tropical biology.

  2. Very cool work! Out of curiosity, I wonder why you choose to use the word “mutualism”, usually reserved for between species interactions. Wouldn’t this within species interaction instead fall somewhere on the cooperation and cheating spectrum?

  3. Terry: This is very interesting, indeed. Simple (i.e., a few interacting species) theoretical models of mutualistic interactions (e.g., Heithaus et al. 1980) are often found to be stabilized by the presence of an antagonistic group (species, population, etc.). I wonder if and how this could be playing a role in your study from both ecological and evolutionary perspectives. In the food hoarding world, we see the phenomenon of reciprocal pilferage (Jansen et al. 2102), where some species cache and pilfer from a common good (seeds) that putatively allows competitively subordinate species to coexist with behaviorally dominant foragers (Price and Mittler 2003, 2006).

    Sarah: Good question. There are many definitions of mutualism in the literature, the most commonly cited and used between species (e.g., Judie Bronstein’s papers below). Many theoretical perspectives from population biology, however, do not necessarily need to make the interspecific distinction and simply study mutualism between two independent units, whether or not they are a part of the same species. I don’t know much about cooperation, but I’d suspect the point at which mutualistic units reproduce (i.e., become dependent) is the point at which cooperation begins, as I think you suggest.

    Thank you for the post!

    Bronstein, Judith L. “Conditional outcomes in mutualistic interactions.” Trends in Ecology & Evolution 9.6 (1994): 214-217.
    Bronstein, Judith L. “Our current understanding of mutualism.” Quarterly Review of Biology (1994): 31-51.
    Heithaus, E. Raymond, David C. Culver, and Andrew J. Beattie. “Models of some ant-plant mutualisms.” American Naturalist (1980): 347-361.
    Jansen, Patrick A., et al. “Thieving rodents as substitute dispersers of megafaunal seeds.” Proceedings of the National Academy of Sciences 109.31 (2012): 12610-12615.
    Price, Mary V., and John E. Mittler. “Seed-cache exchange promotes coexistence and coupled consumer oscillations: a model of desert rodents as resource processors.” Journal of Theoretical Biology 223.2 (2003): 215-231.
    Price, Mary V., and John E. Mittler. “Cachers, scavengers, and thieves: a novel mechanism for desert rodent coexistence.” The American Naturalist 168.2 (2006): 194-206.

  4. Sarah, about ‘mutualism’ – I chose this terminology in the context of potential explanations for the evolution of altruism. (I’m remembering how it was put in the Krebs & Davies Behavioral Ecology text.) I wanted to distinguish mutual benefit from reciprocal altruism. If it’s a ‘mutualism’ then there is some kind of benefit from performing the action that isn’t contingent on a reciprocal act of altruism from the other party.

  5. So, in my understanding, altruism can evolve in 4 very generalizable ways:
    – Kin selection
    – Group selection
    – Reciprocal altruism
    – Sexual selection

    Distinguishing between mutual benefit and reciprocal altruism isn’t necessary, as they are not always directly associated with one another. Instead, if we consider within species interactions in terms of cost and benefits to actors and recipients we can generalize as follows:

    Benefit to actor/Benefit to recipient: Cooperation
    Cost to actor/Benefit to recipient: Cooperation with altruism
    Benefit to actor/Cost to recipient: Selfishness
    Cost to actor/Cost to recipient: Spite

    If we then consider the same type of interactions between species:
    +/+ : Mutualism
    +/-: Parasitism/predation
    -/+: Parasitism/predation
    -/-: competition

    My point here being that this does seem like a very interesting case of exploitation, but that even if there is mutual benefit, that does not necessitate a mutualism which has somewhat different implications (at least from a behavioral ecology perspective- perhaps from a theoretical perspective where you are simply considering ‘entities’ that are interacting, this distinction is less important). I also read back through the Krebs & Davis evolution of altruism section to see if I could find their discussion of the role of mutualisms but was unsuccessful in finding it. Is it located elsewhere?

  6. Terry — I don’t know if you’re aware of it, but there are similar-sounding model systems in yeast. Here’s one paper about it along with the related commentary:

    I run a discussion class on this topic for Masters students so I have a bundle of PDFs of all the key papers if you’d like me to pass them on (and save you time).

    • Markus, I wasn’t aware of this particular set of papers, thanks. With this experiment we didn’t quite have enough data to robustly do the game theoretical models, but we now have another field season and that’s tenable, and an interesting avenue. If someone wants to actually work on this, please let me know! I’m a bit overcommitted (as we all are) but don’t have lab members to whom I can farm this out.

  7. Terry — is there a spatial component to the system? That is, can you fully (and accurately) map the positions of all the relevant colonies and obtain specific estimates of the rates of robbing each experiences (or commits)? If so then I could be very interested…

  8. Markus, we have maps for some of our plots, and for others, we just have distances among colonies. I’d need to go through and tidy things up, but I have a feeling it’d be enough information to get at the questions you’d want to model. (It’s from three separate field projects, led by different people, but a lot of the same measurements.). We should email. But until I get a grant out in a few weeks from now, I’ll be going insane with that….

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