Tales from the Crypt: a parasitoid manipulates the behaviour of its parasite host

I have a new paper out with Dr. Scott Egan, Dr. Andrew Forbes, and Sean Liu! The paper is Open Access in Proceedings of the Royal Society B. Here is the abstract:

There are many examples of apparent manipulation of host phenotype by parasites, yet few examples of hypermanipulation—where a phenotype-manipulating parasite is itself manipulated by a parasite. Moreover, few studies confirm manipulation is occurring by quantifying whether the host’s changed phenotype increases parasite fitness. Here we describe a novel case of hypermanipulation, in which the crypt gall wasp Bassettia pallida (a phenotypic manipulator of its tree host) is manipulated by the parasitoid crypt-keeper wasp Euderus set, and show that the host’s changed behaviour increases parasitoid fitness. Bassettia pallida parasitizes sand live oaks and induces the formation of a ‘crypt’ within developing stems. When parasitized by E. set, B. pallida adults excavate an emergence hole in the crypt wall, plug the hole with their head and die. We show experimentally that this phenomenon benefits E. set, as E. set that need to excavate an emergence hole themselves are about three times more likely to die trapped in the crypt. In addition, we discuss museum and field data to explore the distribution of the crypt-keeping phenomena.

 

Rice University’s videographer Brandon Martin made an awesome video about our study system:

 

 

The absolutely amazing french cartoonist Boulet graciously did artwork illustrating our study system. The study system is a bit complicated, since it’s wasps infecting wasps and it all gets a little hard to follow. Boulet’s artwork does a fantastic job of laying the system out clearly:

 

We were blown away by all of the press coverage of the article. Below are some highlights:

Featured in:

The Atlantic

National Geographic

BBC World

Science

New Scientist (we made the front page!)

Rice University News

Popular Science

Gizmodo

Live Science

The Daily Mail

Phys.org

The Scientist

CBS News

Futurity

Data I’ll never publish II: Salinity and herbivory

I spent a lot of my second year of grad school thinking about salinity and insect herbivory. Generally, insects don’t like very much salt (i.e. how many marine insects have you seen?). Salt is a fairly effective herbivore deterrent – an observation seemingly first made in 1980 by D. Newbery in an Oecologia paper on mangrove herbivory. I made the same observation, and tested it experimentally, in chenopods in a 2014 paper (also in Oecologia – they’ve seemingly cornered the salinity/insect herbivory market).

Coconut palms might be the most widespread and useful (to human) halophytic plant. They were useful for that hammock, at least.  Abaco Island, Bahamas, 2011.

Plants are also affected by salt and have myriad ways to deal with it, basically all variations on either excluding it, sequestering it, or excreting it. Obviously some plants are much better at dealing with salt than others (see mangroves, Zostera, etc.) – we call plants that are adapted to saline environments “halophytes” (i.e. salt plant in Greek). I happened upon a little, weedy, nonnative, and pretty much unremarkable chenopod – Oxybasis glauca – growing at the edge of a building in Davis and somehow I decided it was a pretty cool plant. Given all the other cool halophytes available, I’m not sure why I chose this plant to do a bunch of experiments on, but I did.

This is Oxybasis glauca growing in volcanic sand on the edge of Mono Lake, Mono, CA. I was with a group of about 30 people when I found this and was very excited. I couldn’t really even articulate a single cool thing about the plant – it is salt tolerant, but every plant in that area is salt tolerant. Maybe the coolest thing is that Oxybasis species have really small seeds compared to Chenopodium or Atriplex… maybe there is nothing special about it?

Like most Atriplex and Chenopodium (the genus which Oxybasis was split from) species, Oxybasis glauca has salt bladders – little bubble like trichomes which the plant shunts salt to and then they burst, an odd but effective form of salt excretion. This leaves a layer of salt on the outside of the plant. This protects the plant from herbivory somewhat.

 

Pre- (above) and post- (below) bladder burst O. glauca leaves (lab-grown).

 

Because O. glauca is salinity-tolerant and the primary herbivore of most weedy chenopods in the valley, the spotted cucumber beetle (Diabrotica undecimpunctata), doesn’t like salt (see my 2014 paper), I wondered if there might be a refuge from herbivory effect at higher salinities and maybe there would be an intermediate salinity where the plant would still grow well, but herbivores would be deterred. So I did an experiment – I grew plants in three salinities* and then exposed half of them to a week* of cucumber beetle herbivory. I expected herbivore pressure would be most intense at low salinities, but also growth would be retarded at higher salinities.
So the hypothesis looks something like this – if plant “performance” is on the y-axis and the green line is effect of herbivory and grey the effect with solely salinity, if there is some overlap, the plant might do best at that overlap point (or it might not). (note: this is not a particularly good graphical representation for a number of reasons).
What did I find?
Plant response to salinity (w/o herbivores):
Salinity increasing left-right. Standard deviation plotted.
Plants did worse as salinity increased (as expected).
Herbivory:
Salinities increasing in treatments 1-4. Standard deviation plotted.
Total leaves damaged by the herbivores decreased with increasing salinity (as expected, as they are less palatable), but because the plants had fewer leaves, the proportion damaged increased.
THE INTERACTION
Biomass of plants. Dark green: with herbivores, light green: without herbivores. Salinity increasing left to right. Standard deviation plotted.
Sadly, there wasn’t. Beetles didn’t really have an effect on biomass (or any other metric). Maybe I didn’t have them in there for long enough? Maybe they really don’t have a fitness effect (I can certainly believe this).
Maybe this data will be useful to someone. Email me for the sheets.
*Note: the exact procedures are in one of about 40 notebooks in my office, so I don’t actually know exactly the salinities or number of days right now. If anyone is interested for any reason, I can easily dig this up.

An unexpected herbivore

Columbines are toxic! Like larkspurs, columbines are supposedly toxic to most livestock and humans. So say the books. This rabbit doesn’t listen to the books. (The internet, in its infinite wisdom, says that the eastern species has edible – to human – flowers, so maybe the rabbit is just rather tech-savvy)

I actually suspect that the roots and leaves may be somewhat toxic but the reproductive parts, including the flowers and pedicels (which the same rabbit eats in the next video!), are not. Deer also eat them, especially in one particular population, which I’ve mostly stopped using for experiments because of it. Wild speculation aside, just thought I’d share the video as I got a kick out of it.

Also, a question – is this a brush rabbit (Sylvilagus bachmani), a European rabbit (Oryctolagus cuniculus) or a black-tailed jackrabbit (Lepus californicus)? . A terrible still of the tail from the video is below. I feel a bit silly that I can’t even conclusively get it to genus. I’d be kicking myself pretty seriously if I couldn’t get a dragonfly, bird, wildflowers, or butterfly to genus and really this should be far easier!

 

A natural history idea for ecologists: the natural history supplement

At risk of rehashing what is in this very short paper (open access pdf here), a few colleagues and I have a simple idea for how to encourage natural history in current ecology and evolution. A whole bunch of notable folks, including Harry Greene, Josh Tewksbury, Paul Dayton and more have noted the decline in traditional natural history – the taking of observations, collecting specimens, and classes in zoology and botany – among academics over the last half decade or so. Their papers all deserve a read as they point out very real problems and quantify these declines.

Though these papers draw attention to the issue and make a very convincing case that it is an issue, they don’t offer realistic solutions. I’ll not overstate our case; our small idea won’t bring back botany classes where they once were taught or inspire people to create an insect collection at a college without one. However, we have an idea that may incentivize natural history study, at least a small bit. We propose that ecologists and evolutionary biologists create a natural history supplement with their paper to highlight potentially interesting observations and important natural history data.

An example of character displacement? A somewhat disjunct population of Abronia pogonantha in the coast range (left) is deep pink-purple, where populations I’ve looked at in the Mojave which grow near Abronia villosa (a deep pink purple species) are whitish or very light pink (right). I’m not going to investigate it, but I’ll include it in a natural history supplement so someone else might and I took specimens of these plants and sent them to an herbarium.

Anything of potential interest could go into this supplement (though it should not be used as support for the main assertions of a paper – any natural history of that sort still belongs IN the paper). This needn’t only apply to field studies, either – researchers working in greenhouses or in laboratories with colonies of microorganisms make important natural history observations, too – they are just as intimately familiar with their study systems as a field biologist.

We think that there are a few reasons why this small addition would be particularly important and useful. First and most obviously, these observations WILL be useful to someone down the line, somewhere, sometime. Even if it takes 50 years for someone to investigate a particular plant or insect, these observations of behavior, population size, flowering time, etc. in 2016 are an invaluable snapshot of what you saw when. Richard Primack and co.’s wonderful reanalysis of flowering time data which Thoreau gathered in the 1800’s are a perfect example of this type of use. Secondly, meta-analyses and comparative studies are commonplace and particularly informative and could use those life history data included in these supplement that wouldn’t make it into a paper on another aspect, but are likely data that many folks take instinctively.

Since we have the internet, archiving these sorts of things has never been easier. Many papers have a great deal of supplementary information (especially in short-form journals) and publishers have ways to archive it. While it doesn’t need to be done immediately, if this practice is adopted, a database of these natural history supplements could be compiled at any time.

This caterpillar, Sympisits [Lepipolysperscripta, is having a good year on both Antirrhinum vexillo-calyculatum (pictured) and A. cornutum. However, it is far more abundant on v-c. even when cornutum is the more abundant food. I’ll likely never write a paper on snapdragons, but if I did, this would be a perfect type of observation for the natural history supplement. 

Lastly, it incentivizes natural history observations and data. The “currency”, if you will, of academia is papers and citations. While including a natural history appendix doesn’t boost the first aspect, if the additional information in that supplement is of use to others, it can only boost your citation count and make your work more widely read.

If those sound like good or bad arguments, read the full paper (again, here), there is a good bit more in it. I’ll conclude by saying that I’ve written two of these, both for papers in Ecology (here and here) and they have been easy and enjoyable to write. Has anyone actually read them? I’m not sure (do tell if you have!). Maybe not, but that doesn’t seem particularly troubling to me – even if one person reads them and gets inspiration for a study or uses some data in an analysis decades after I’m gone, I’ll be happy. Plus, they were more fun to write than the main text of these papers. I focused both of these by describing briefly a great deal of natural history, hoping that someone studying one of these systems (especially the well-known ones, like Mimulus or Petunia or Nicotiana) would think about insect- or sand-entrapment.

On another level completely, I’m sure Ecology wouldn’t have let me use the fantastic quote “[Pholisma feels like] a squishy gummy bear covered in fuzzy sand covered hairs” in the main article 🙂 .

This stilt bug, Jalysus wickhami, moves easily on the sticky surfaces of many plants, including this weird, sticky fire-following monkeyflower, Mimulus bolanderi, by grabbing the glandular trichomes below their sticky heads. However, when I perturbed it for this photo, it got a bit of the sticky stuff on its front legs (visible in photo) and was visibly disoriented and had to groom it off with its other legs. Some cool papers have focused on movement on sticky plants, so the trichome grabbing behavior is well-known, but I might still include this in a supplement (with proper citations to those papers, of course).

Postdoc with Dr. Ryan Hechinger (and me!)

We’re looking for a postdoc! See below!
——————
Postdoctoral Opportunity with the Marine Biology Research Division at SIO
Postdoctoral Scholar – Employee
Academic Division: Scripps Institution of Oceanography
Academic Department/Research Unit: Marine Biology Research Division
Disciplinary Specialty of Research: parasitology, physiology, behavior, fish, birds, ecology, estuaries
Description: The position will involve taking on a 1.5 year project in the Hechinger Lab at Scripps Institution of Oceanography, University of California, San Diego. The project is part of a larger, international project. Collaborators include Dr. Øyvind Øverli (Norwegian University of Life Sciences) and Dr. Kelly Weinersmith (Rice University). The overall project weds parasitology, ecology, behavior, neurobiology, and omics. This post-doc will examine the impacts on estuarine birds by Euhaplorchis californiensis, a trematode parasite. The parasite uses birds as final hosts, but effects there are countered to unknown extent by the parasites modifying the behavior of the birds’ prey, the California killifish, making them easier to catch.
The current plan is for the post-doc to be lead a laboratory study using controlled exposures of final hosts (birds, rodents) to document the parasite impacts on those hosts. Impacts will be measured at least by growth rates and, likely, metabolic rates (respirometry). The post-doc may also be involved with other aspects of the project, including a field experiment using fish in enclosures to quantify how fish infection changes bird predation rates and success.
Salary/Stipend Information: NIH standard & based on years of postdoc experience
Qualifications and preferred academic background: Candidates should possess some or all of these attributes (some of which, including parasitological skills, can be learned on the job):
1. Ability to handle, maintain, and dissect birds and rodents.
2. Ability to do respirometry on air breathing vertebrates.
3. Ability to dissect fish, birds, and rodents, and quantify parasite abundance and body size.
4. Have good communication, organizational, collaborative skills.
5 viagra quebec. Have solid analytical skills. At least a working knowledge of general and generalized linear models. Dynamical modelling skills are a plus, but not required.
6. Proven writing/publication skills as indicated by published papers.
7. Experience or ability to deal with live, wild estuarine birds.
Appointment Length/Period: Appointment will start as early as 1 August 2016 and continue for 1.5 years.
Application procedure: Send an email with subject header “POST-DOC APPLICATION”, with an attachment of a single PDF file that includes a cover letter, CV, statement of research interests, and contact information for three references to Dr. Hechinger at rhechinger@ucsd.edu.
Application Closing Date: 24 Jun 2016