Relationships involving a “household of three” hold a fascination that is part prurient and part wonderment: prurient for perhaps obvious reasons, and wonderment as it’s sometimes hard enough to make a ménage à deux work! Historically this domestic arrangement has been the lifestyle of choice of a surprisingly large and diverse set of influential thinkers and creative individuals, including Aldous Huxley, Lord Nelson, Carl Jung, Erwin Schrödinger, and Hattie Jacques. Indeed, one of my favourite musicians, David Crosby, wrote a song about such relationships (Triad) which got him kicked out of The Byrds.
In nature, ménage à trois are occasionally encountered and may be more common than we think, and have been on my mind because this week I’ve been talking about mutualistic relationships with my first year undergraduates. Mutualisms are interactions between species in which both benefit, as opposed to exploitative relationships such as predation or parasitism in which one of the partners is at a disadvantage (being eaten is a great disadvantage….) Mutualistic interactions are common and important, and include many (but not all) plant-pollinator interactions, seed dispersal by birds and other animals, mycorrhizal relationships between plants and fungi, and many more. As well as studying plant-pollinator interactions, I’ve a long-standing interest in the full breadth of these examples of “biological barter“, in all their varied forms.
In most cases mutualistic relationships involve pairs of species (for example a plant and a pollinator) although these species pairs are embedded within a larger network of interactions: that plant may have many pollinators, and those pollinators may service other plants. In this sense it requires just two partners to make the interaction work – a “household of two”. More rarely, research on the biodiversity of species interactions throws up examples of “households” involving three species, and a fascinating case has recently been worked out and published by Jonathan Pauli and colleagues. This involves three-toed sloths and their relationship with the algae and moths that colonise the sloth’s fur – you can read the abstract here. In summary, the algae benefit from nutrients provided by the moths living in the fur; the sloths eat the algae to supplement a restricted diet of leaves; the moths benefit from the sloths transporting them to defecation sites where they lay their eggs, then recolonise the sloths. This slothy ménage à trois is a wonderful instance of interdependency within nature.
The other case of a three-part mutualism with which I’m familiar is that between anemonefish, and sea anemones and the algae which are housed in their tentacles. The fish and the anemones provide mutual defence of one another, whilst the algae photosynthesise and provide carbohydrates to the anemone, and benefit from the nitrogenous waste produced by the fish. It’s a system that I’ve done a little work on with marine biologist colleagues, specifically the broad scale biogeography of the interaction and its local assemblage structure, but we’ve not studied the whole three-part system.
What other three-part examples are there in nature? I’d be very interested to hear about any of which you’re aware.
It begs a question as to whether three is an upper limit to the number of species that can engage in such relationships? Are there any four- or five-part mutualisms? Or are these too unstable over evolutionary time, because if one species goes extinct it could cause the extinction of other species? Interesting questions about fascinating interactions!
Prof. Jeff Ollerton - ecological scientist and author 
Interesting idea… I wonder if there are some yeasts/bacteria living in flowers nectar, which get a clear benefit from the plant, but also help the plant attract pollinators (by producing -OH or aa, maybe?), adding that way the third partner to pollination mutualism. I think I read something about it somewhere, but my memory if failing today.
Also, after reading your post I start seeing plant-pollinator networks as a big mutualism orgy.
Yes, possibly, that’s an interesting point; I know that Carlos Herrera has done some work on the yeasts in nectar. I’ll look into it.
As for the “big mutualism orgy” remember that in its strict sense, a menage a trois is not the same as a threesome 🙂
Oh oh definitely the vegetarian spider! http://standingoutinmyfield.wordpress.com/2011/12/12/the-vegetarian-spider/
PS I wrote that post a long time ago, don’t judge.
I never judge, I only comment 🙂
Hmmm, maybe I’m missing something, but how is the spider’s activities mutualistic for the ants or the plants? Isn’t it just parasitising the existing two-way mutualism? It’s an interesting interaction but I don’t think it’s what I had in mind 🙂
Also, how about the phoretic cryptophagid beetle that hitchhikes on bee tongues?
Ditto previous comment – all three species have got to be directly mutualistic to one another.
Oh that is so much tougher…I will think some more.
Okay, here is one I have thought of…feel free to shoot it down, but I was thinking the gut contents within the rumen of a cow? There is a mutualism between the cow and its gut symbionts, but within the gut there is a complex community. Some of the bacteria produce by products that feed the yeasts, which feed the fungi, and so on. What do you think?
Yes, that’s certainly a possible one, though I don’t know of any studies that have worked out the details of the benefit pathways.
Them’s the rules 🙂
Okay two more tries, with papers to back it up. The bug within a bug within a bug: http://phenomena.nationalgeographic.com/2013/06/20/snug-as-a-bug-in-a-bug-in-a-bug/
(and the scientific paper: http://www.cell.com/retrieve/pii/S0092867413006466?cc=y)
Ant-fungus garden-bacteria: http://www.esf.edu/efb/schulz/seminars/currie.pdf
(another paper: http://www.plosone.org/article/info%3Adoi%2F10.1371%2Fjournal.pone.0008748)
Ah, I knew the Currie et al.ant-fungus-bacteria paper, but had forgotten about it. The other is a new one for me though. Excellent, thank you, we’re building up more and more examples. Still no sign of a four-way mutualism though….. 🙂
Ah!
There’s a nice piece about the sloth story in the New York Times: http://www.nytimes.com/2014/01/28/science/the-sloths-busy-inner-life.html?_r=0
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