Monday, September 26, 2016

Musings on pollinators and sticky plants

Having spent much of the last four years seeking out sticky plants, I'll admit to mostly having thought about their herbivores and general insect communities on the plant surfaces, without too much thought to pollination. A labmate's question about columbine (Aquilegia eximia) pollination - "Do they have any adaptations to prevent bees?" got me thinking about this. A. eximia is hummingbird-pollinated and is extremely sticky (see here). I've spent enough time looking at, and photographing, over a hundred species of sticky plants that I was able to dredge up some pertinent observations (some from field notebooks) and I'll reference a few papers that have mentioned this.

A honeybee entrapped on the sticky flower/pedicel of serpentine columbine (Ranunculaceae: Aquilegia eximia). Note the robbing hole present on the front (out of focus) and left spur. These were made by carpenter bees (Xylocopa californica). Honeybees and other bees visit as secondary robbers, though they do not regularly visit unrobbed flowers. The primary pollinator of A. eximia here is Anna's Hummingbird (Calypte anna).  McLaughlin Reserve, Lake County, CA. 
The general explanation for sticky plants is that it prevents herbivory directly (by slowing or entrapping herbivores). This is generally an insufficient explanation, as pointed out by Tom Eisner and colleagues (here) who found that ladybugs were slowed or entrapped, allowing a specialist aphid to feed on Mentzelia pumila (Loasaceae - a painful plant family). Eisner's explanation, however, also seems simplistic and incomplete - it turns out that a suite of specialist predators are good at moving on sticky plants and do effectively prevent herbivory (here, herehere, more coming!). Whether these are exceptions or the rule, I suspect this defense is fairly common. While I think Eisner et al. missed the boat on trophic relations in Mentzelia (this is not a completely baseless accusation; I have some data to back my case up), they do make an astute observation on a cost of being sticky: "among the insects we found dead on M. pumila there were several individuals of an andrenid bee, Perdita sp., ... a genus known to include pollinators of Mentzelia. Evidently the trichomes can be a hazard to [pollinators] ".

People have long thought about adaptations both for a specific pollinator and against others that are not as effective. Is stickiness a problem for pollination or could it be a benefit in some cases?

Entrapped Lycaenid butterfly (I think it is Plebejus acmon) on Mentzelia micrantha. It seems likely this butterfly was entrapped while visiting a flower, as it is entrapped on a flowerhead (it is on a bract surrounding a fruit, but it probably had been there since there was a flower). Napa County, CA.
First, we should ask: do sticky plants actually entrap their pollinators commonly? Unlike the smaller-flowered Mentzelia (like micrantha pictured above), which are likely self-pollinating, the larger-flowered species, including Eisner's pumila (and the widespread and stunning laevicaulis) have large flowers separated from the very sticky (like velcro) leaves. Carnivorous plants, including the sticky sundews, often have widely separated flowers and traps. Yet, a nice study by Jurgens et al (here) found that the separation in one sundew is simply because taller flowers attract more pollinators (and the sundew's sticky leaves remain near the ground). They found that the color differences between the flower and trap were more important in keeping pollinators on the flower and off the leaves. Complementing this, a more recent study showed that color is important, but odor might also be important, especially in sundew species without much physical separation (here). A strange paper (see footnote) on a South American aster showed practically no overlap between pollinators and entrapped insects (here). The sticky columbines - eximia, shockleyi, and some populations of formosa - are all hummingbird-pollinated, as is the sticky monkeyflower, Mimulus cardinalis; the chance a hummingbird becomes entrapped is virtually zero. 

The first thing to note is that none of these papers have actually examined whether there is a pollination cost to being sticky. Of course, a past cost may shape evolution, but not be obvious now. While these examples make the case for putative adaptations to not entrap pollinators, none except El-Sayed's paper have any sort of comparative aspect. Therefore, we can't be sure that these are actually adaptations. This isn't to belittle the research, of course, as the experimental studies are very nice and convincing that these factors underly the non-trapping of pollinators.

A small bee of some sort entrapped on a serpentine columbine bud. Two Tupiocoris californicus, one of the mutualistic predators, are pictured on the right of the bud. McLaughlin Reserve, Lake County, CA. 

I wonder, if perhaps in addition to these chemical and visual cues keeping pollinators away, if another way to avoid entrapping pollinators is to utilize pollinators which are too large to be entrapped? Could it then be used to exclude suboptimal pollinators? Might stickiness might be easier to evolve in plants with larger pollinators or sticky plants be selected on to have larger pollinators? This chicken-or-egg situation need not be resolved; it would be interesting enough to find out whether there is a correlation. One could go about testing this by looking at insect-entrapping plants and comparing them to their close relatives and asking (quantitatively), is the pollinator of this sticky plant larger than expected given the pollinators of its closest relatives? Our paper on columbines includes a genus-level list of insect entrapping plants, this would be a good place to start when looking for possible comparisons (at whatever level you choose, you'd need to have both sticky and non-sticky members of each taxa). Off the top of my head - Aquilegia, Mimulus,  Salvia, Calceolaria, Ribes, Nicotiana seem like genera with both sticky and nonsticky members and pollinator variation and would be a good place to start (surely I am missing some).

A small solitary bee (I'm not good on bee genera) on Mimulus bolanderi. Among Mimulus that I've investigated, bolanderi entraps the most insects. There is little information on this strange, fire-following species, and I have only seen one pollinator visit (this one!), but I was mostly looking for predators. Another insect-entrapping Mimulus is hummingbird-pollinated (cardinalis). Some populations of common monkeyflower (M. guttatus) are sticky, others are not - all are bumblebee pollinated, I believe.
In conclusion:

1) Sticky plants occasionally entrap potential pollinators, though we don't know yet whether there is a realized cost to this, indeed it could be a benefit and may keep less-effective pollinators away.

2) Several experiments have demonstrated that features of some sticky plants prevent pollinators from being entrapped.

3) I hypothesize that sticky plants may have larger pollinators, as it would reduce chance of a cost (but I am agnostic about which might evolve first) and might even have a benefit (as an adaptation to exclude some pollinators).

I'd love other people's thoughts or other references (I haven't really dipped my toes into the literature on keeping less effective pollinators out of flowers).




Footnote:
I hope this group follows up on this system, as cool questions could be asked, but this paper is confusing (and if they read this post, they should read Patricia Thomas's 1988 dissertation at U. Illinois, which looks at a similar system in a thistle - I have a pdf). They looked at Haplopappus flowers, which have sticky bracts (like Grindelia and some Cirsium) and recorded flower visitors and entrapped insects to see whether there was overlap. This, in and of itself, is a good exercise. However, the paper is lacking in much pertinent information and clear discussion of what they found, What stuck out to me most was that they found that the tephritid fruit fly, Dioxyna chilensis, (which is an herbivore of this plant) was a common flower visitor and commonly entrapped, thus the stickiness may be a direct defense. Somehow this and really any herbivory isn't mentioned - despite "herbivores" being mentioned in the title - herbivores weren't really discussed in the paper. Also, they discuss pollinators, but not really any functional explanations of why some insects might end up on bracts and others on flowers (for instance, they found ants and a family of beetles were the most commonly entrapped insects - yet they don't discuss that both primarily walk, whereas the non-entrapped taxa fly). Their conclusions are technically right, but rather incomplete: "Thus, comparing all arthropod genera found, it seems that bracteal resin selectively traps insect genera with lesser pollen transfer potential." Hopefully more work will come out, as it seems Villagra's lab is working more on the system.