Tasty truffles tempt mammalian dispersers

The first humans known to eat truffles were the Amorites (Old Testament victims of Joshua during his Canaan conquest) over 4000 years ago.  Many other animals eat truffles as well; in fact humans commonly use dogs (and sometimes pigs) to help them locate truffles, making good use of their highly developed sense of smell. Apparently pigs and perhaps dogs as well, need to be muzzled so that they don’t consume this delightful fungal delicacy following a successful search.

Ryan Stephens was studying the small mammal community in the White Mountains of New Hampshire as part of his doctoral dissertation, and was particularly interested in what these mammals were eating.  It turned out that fungi comprised about 15% of the diet of the woodland-jumping mouse, white-footed mouse, deer mouse and eastern chipmunk, and about 60% of the diet of the red-backed vole. So he and his colleagues began surveying truffles in the region, and discovered several new species in the process.  

New Hampshire’s White Mountains. Credit: Ryan Stephens

The Elaphomyces truffles we will discuss today are partners in ectomycorrhizal associations.  The fungal hyphae form a sheath around the roots of (primarily) Eastern hemlock trees providing soil nutrients to the tree in exchange for carbohydrates created by the tree’s photosynthetic processes.  What we call “truffles” are actually the fungal fruiting bodies, or sporocarps, which upon maturing develop massive numbers of spores that must somehow be dispersed.  This is a problem for an organism that is attached to underground tree roots.  The solution that has evolved in truffles is emission of volatile substances that communicate with truffle-loving mammals, informing these mammals where the truffles are, and that they are ripe and available.  Mammals dig the truffles up, eat them, and then defecate the spores in a new location that may be many meters or even kilometers away.  

Sporocarps (fruiting bodies) of the four truffle species used in this research. From left to right: (a) Elaphomyces americanus, (b) E. verruculosus, (c) E. macrosporus, (d) E. bartletti. In each photo one truffle has been cut in half, revealing the spores and the spore-bearing structures.

At the Bartlett Experimental Forest in the White Mountains, Stephens and his colleagues set up 1.1 ha grids at eight forest stands that were rich in Eastern Hemlock. Within each grid, they set up 48 16m2 sampling plots for truffle collection.  They used a short-tined cultivator to dig up all truffles within each plot, counting, drying and weighing each sporocarp, and then analyzing each sporocarp for %N. Using simple arithmetic (and some assumptions), the researchers were able to convert %N to % digestible protein.

Short-tined cultivator in action, uncovering two sporocarps. Credit: Ryan Stephens.

It was impossible to measure the depth of each sporocarp, because raking the soil disturbed it too much for accurate measures.  Instead Stephens and his colleagues took advantage of previous research that discovered that soils dominated by ectomycorrhizal fungi have a specific pattern of how a stable isotope of heavy nitrogen (15N) is distributed in relation to the normal isotope (14N), with higher 15N concentrations the deeper you go. The sporocarps have similar 15N concentrations as the soil around them (actually slightly higher, but in a predictable way), so a researcher can measure the 15N/14N ratio of a sporocarp, and estimate its depth in the soil column.  

Stephens and his colleagues discovered that Elaphomyces verruculosus was, by far, the most abundant truffle (Figure a below).  Sporocarps of the four species occupied very different depths, with some overlap (Figure b).  E. verruculosus and E. macrosporus had more digestible protein than the other two species (Figure c).  Lastly, all species had similar sized sporocarps (Figure d).

Sporocarp (a) abundance, (b) depth in soils, (c) % digestive protein and (d) dry mass across the sampling grids. Thick horizontal line in box plots are median values, box limits are first and third quartiles and notches are the 95% confidence intervals. The vertical lines above and below each box extend to the most distant data point that is within 1.5 times the interquartile range.

If a truffle’s sporocarp is deep below the soil surface, we might expect it to emit a stronger chemical signal than a sporocarp nearer to the surface, so it can attract a mammalian disperser.  Having a fully equipped chemical laboratory allowed the researchers to measure the quantity and type of chemical emitted by each species.  They discovered that E. macrosporus and E. bartletti, the two deepest species had the strongest chemical signals – emitting relatively large quantities of methanol, acetone, ethanol and acetaldehyde.

Field research team of Andrew Uccello, Tyler Remick and Chris Burke – each has handsful of E. verruculosus sporocarps. Credit: Ryan Stephens.

The question then becomes, which truffle species are small mammals most likely to eat?  If they go for the easiest to reach, they should prefer E. americanus.  If they go for the most nutritious, they should prefer E. verruculosus and E. macrosporus.  But if they prefer the ones with the strongest signal, they should focus their attentions on E. macrosporus and E. bartletti.

On the surface you might realize that it is difficult to figure out who is eating what.  This is true. To address this problem, the researchers analyzed the quantity and type of fungal spores defecated by mammals that were captured in live traps within their research grids.  Analysis of the feces indicated a consistent preference among all five species of small mammals for the two truffle species with the strongest signals, even though that resulted in them needing to do a bit of extra digging.  The only exception to that trend was red-backed voles consumed much more E. verruculosus than did the other mammals. Recall that E. verruculosus was one of the most nutritious truffles, and that fungi comprise more than 60% of a red-backed vole’s diet. So it was more important for that species to discriminate based on food quality.

Truffle selection by small mammal community. N. insignia = woodland jumping mouse , P. maniculatus = deer mouse, M. gapperi = red-backed vole, P. leucopus = white-footed mouse, T. striatus = eastern chipmunk. Jacob’s selection index measures consumption relative to the availability of each truffle species, with +1 representing strong preference and -1 representing strong avoidance of a particular truffle species. Error bars represent 95% confidence intervals around the mean.

Why don’t the shallow truffle species emit stronger signals? One possibility is that a shallow truffle with a strong signal might get harvested and eaten before it is fully mature, and does not yet have viable spores. A second possibility is that shallow truffles might rely on soil disturbance or mammal activity (burrowing or just scurrying by) to make its way to the surface.  Upon reaching the surface, its spores can disperse in the wind like the spores of more traditional mushrooms. It requires considerable resources to produce these volatile compounds, so a truffle should only produce them if they are highly beneficial. Thus a stronger, energetically costly signal might not be necessary for the shallowest truffles, and may even be counterproductive.

note: the paper that describes this research is from the journal Ecology. The reference is Stephens, R. B.,  Trowbridge, A. M.,  Ouimette, A. P.,  Knighton, W. B.,  Hobbie, E. A.,  Stoy, P. C., and  Rowe, R. J..  2020.  Signaling from below: rodents select for deeper fruiting truffles with stronger volatile emissions. Ecology  101(3):e02964. 10.1002/ecy.2964. Thanks to the Ecological Society of America for allowing me to use figures from the paper. Copyright © 2020 by the Ecological Society of America. All rights reserved.

One thought on “Tasty truffles tempt mammalian dispersers

  1. Hi Fred Just got around to reading your latest. I always enjoy your writing and delightful intros and humor (“This is a problem for an organism that is attached to underground tree roots.”). This was a fascinating investigation in a variety of ways. 1) the huge amount or work that seemed to be involved. 2) the technology they could muster to address the question. 3) their ingenuity (and thanks for the reminders about assumptions), and 4) By the end I was wondering what the average Joe would be asking about the benefits of this research to anyone – and whether he was footing the bill with his taxes 🙂 chuck ________________________________________

    Like

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