You might be familiar with the Janzen-Connell model, that was covered in Annals of Botany recently. If not here’s a quick recap.
Janzen and Connell were both working on the same problem. How do you get diversity of trees in forests? Why doesn’t one tree dominate? The answer, they independently proposed, was down to predators. If you get a bunch of similar trees, then it’s a convenient all-you-can-eat buffet for anything that likes that tree’s seeds. So successful trees attract enemies that eat the seeds, and so the trees are kept in check. Kept in check might be understating the problem for the trees though. Trees can lose a lot of seeds to predators. The recent Annals paper said between 70%-100% of seeds can be lost to creatures eating the seeds. A meta-analysis found real-life was a bit more complicated than that, but the Janzen-Connell model holds up. Successful tree populations attract attackers.
For the Mongolian oak, Quercus mongolica, a problem comes from Curculio weevils. The female weevil has an elongated nose, called a rostrum. She uses this nose as a drill to bore into acorns and deposits eggs inside. These eggs become larvae that eat the acorn from the inside -out. Becoming a weevil nursery is bad news for the oak, as the energy invested in the acorn is lost. If weevils infest the whole tree, then reproduction is impossible. So, given the problems, you might not think that an oak would benefit from attracting granivorous (seed-eating) chipmunks.
A new paper by Yang and colleagues investigates this, and finds that while it might look like chipmunks eat acorns (because they do), they’re a third partner in the oak-weevil battle and they give more aid to the oaks than the weevils.
The authors identify the chipmunks as Tamias sibericus, the only chipmunk in Eurasia. The common name is the Siberian chipmunk, though they’re found in many places outside of Siberia. They behave a bit like squirrels. They like seeds and grains, and they also cache food as well as eat it. It’s this caching behaviour that’s so important for the oak. For a start the chipmunks carry away seeds away from the weevil infested area, bury the acorn and then (some) get eaten by a passing hawk, leaving the acorn to grow in possibly a less harmful environment – but they also do much more. To the chipmunk not all seeds are equal.
From the chipmunk’s point of view, it wants to think that when it comes back to the acorn, it’s going to be edible. Weevil infested acorns will be eaten by the time the chipmunk is ready to feed, so what does the chipmunk do to improve storage? Yang et al. gave a bunch of chipmunks some infested and uninfested acorns and then watched to see what they did with them. Chipmunks like acorns, so it’s no surprise that some acorns were eaten straight away. They like eating in a safe place, so some acorns were taken away and eaten. Also, they like to cache, so it’s no surprise that some acorns were taken away and buried.
The actual figures were striking. About 60%-70% of acorns were eaten at the feed site. A few, but not many, were taken away and eaten. Roughly 20% of the acorns were taken for caching. However, the fate of the acorns differed depending on whether they were weevil infested or not.
If an acorn had weevil larvae, then there was more than an 80% chance that the chipmunk would eat it straight away. They ate weevil larvae when they were offered them too, so it seems chipmunks have no problem with extra protein. In experimental settings, the chipmunks were just as likely to take away a healthy acorn and hoard it as they were to eat it. For the infested acorns in the experiment, it was pretty much a choice between eat or reject. The chipmunks didn’t waste any effort on caching the infested acorns.
The difference in caching makes sense from a preservation perspective, Yang and colleagues wondered if there was more to it. They found there might be some differences in volatile compounds given off by infested acorns compared to the healthy acorns. Did this affect the success of caches? Once you bury them, it might not be just you who comes looking for them. So they tested the ability of the chipmunks and some Korean Field Mice, Apodemus peninsulae, to find and raid caches of nuts. I like the idea that infected nuts release volatile gases as a perfume to attract predators, and encourage animals to only cache healthy seeds. So I was disappointed to find there’s no evidence that infestation helped rodents find acorns. It appears that the shell is more of a source of scent, explaining why chipmunks shelled acorns before caching.
Oddly, shelling the nuts before caching did help with preservation and reduced the chances of fungal attack for the acorns. So despite being seed predators themselves, the chipmunks did plenty of work for the oaks in dispersing acorns and improving survival chances of healthy acorns. The chipmunks are less effective predators than the weevils, so there could be substantial advantages for oaks to attract chipmunks, particularly when weevils strike. Unfortunately, as the authors note: “The null hypothesis that shelling by T. sibiricus has no effect on cache loss and seedling establishment could not be rejected on the basis of our study.”
While the experiments don’t all give clear results, they’re written up in ways that others can use. There’s plenty of interest in multi-level trophic interactions, and the idea that plants encourage predators of predators is well-established. With plenty of plant-pest-rodent interactions around the world, while this study focuses on a relationship found in China, it has relevance to research across the planet.
Xiao, Z., Mi, X., Holyoak, M., Xie, W., Cao, K., Yang, X., … Krebs, C. J. (2016). Seed–predator satiation and Janzen–Connell effects vary with spatial scales for seed-feeding insects. Annals of Botany, 119(1), 109–116. https://doi.org/10.1093/aob/mcw224
Comita, L. S., Queenborough, S. A., Murphy, S. J., Eck, J. L., Xu, K., Krishnadas, M., … Zhu, Y. (2014). Testing predictions of the Janzen-Connell hypothesis: a meta-analysis of experimental evidence for distance- and density-dependent seed and seedling survival. Journal of Ecology, 102(4), 845–856. https://doi.org/10.1111/1365-2745.12232
Yang, Y., Wang, Z., Yan, C., Zhang, Y., Zhang, D., & Yi, X. (2018). Selective predation on acorn weevils by seed-caching Siberian chipmunk Tamias sibiricus in a tripartite interaction. Oecologia. https://doi.org/10.1007/s00442-018-4161-z