A Caterpillar Mystery in the Bahamas

I've been in the Bahamas for the last two weeks, studying the effect of resource pulses (hurricane-wrecked seaweed) on island communities with this project. In doing so, we kept coming upon these strange shelters on wild guava (Psidium longipes), locally called Bahama stopper, since the hard wooded bush/tree would apparently stop any progress you try to make into the thick coppice.

What on earth is this? ~  4 cm tall (pretty damn big by insect standards).

Inside some of these shelters (2/13), there was an odd larva, apparently a beetle larva, or so I initially thought. Because I am mostly a caterpillar person, I didn't really pay it much mind. 

A really terrible picture, but notice the "antennae". About 2-3 cm long. 

Louie, while processing insect samples one night, noticed that some things were not right about the apparent beetle larva - namely it had prolegs, the fleshy appendages that give caterpillars the appearance of having more than the six legs all insects have. I then looked at the "antennae" and found that they were not segmented, a dead giveaway that this was, in fact, a caterpillar and the "antennae" were actually tentacles (yes, that is the technical term for the fleshy projections that many caterpillars have - monarchs for instance).

Several of the shelters were torn like this, suggesting predation (by a bird [?]). This was the
only shelter with lines affixing it at the top - many had lower lines. 

I got much more interested after that, and sent along these pictures to Charley Eisemann, a good friend and probably the person on earth with the most knowledge about insect shelters. His blog - linked above - is simply phenomenal and if anyone was going to know the answer, he would. Very quickly (within a few minutes), he had correctly found the family of the moth - Mimallonidae. The amazing part here is that Charley has never seen a member of this family! Mimallonidae is an extremely small family by Lepidoptera standards, ~200 spp. - only 3 of which occur regularly in the US, a fourth is described from the US in Brownsville, TX, but is probably a tropical stray. He even dug pretty deep and found a very likely species identity, Ciccinus packardii - known from Cuba and known to feed on other Psidium species. While I do not know this for sure, it seems that is the most likely candidate as the larva matches very well the few images of Ciccinus online, and less so the other mimallonid genera. 

After a bit more searching, we came upon a young larvae feeding in a leaf press on P. longipes, which was not what I expected. This family is known as the "sack-bearers" and I was expecting something more along the lines of a bagworm (Psychidae), instead of a leaf presser.

A young (2nd, 3rd instar?) larva of this Ciccinus sp. ~ 8mm

Which brings us to the strange, pitcher plant-like shelters. The larva is oriented vertically inside the shelter, with a strange butt plate plugging up the bottom hole and the head just below the upper hole. What function the little hood forms is mysterious - perhaps shading the larva from the hot Bahamian sun or fierce rains? The better-known Ciccinus species of the US, C. melshiemeri, feeds on old oak leaves (too tannic for most caterpillars) and constructs a shelter, sort of like the pictured ones of frass pellets, silk and oak leaves in which it spends the winter as a larva, prior to pupation in the spring. This seems to be the case for this species as well - in two cases, I found spent pupal skins.

Spent pupal skin (successful emergence!) inside one of the shelters. You can also see the construction of silk and what
appears to be finely ground frass (caterpillar poop - a common building material for cats). 

Interestingly, I did find one that fit the description of the C. melshiemeri shelters well.

This was the only shelter anchored into leaves (it was vacant, unfortunately). You can see well the frass pellets forming the top of the shelter here.

The same shelter, with a Psidium leaf forming one side. 

These guys kept me occupied for quite awhile (I even dreamt about them!) and seem like a worthy avenue for future rearing efforts... there are a great deal of questions that remain about the shelters: Why the strange shape with a hood? Why build a free standing shelter, as opposed to anchoring it to a stem like most moths? Why wait around in a shelter instead of pupating right away? Do the shelters protect inhabitants from predators and parasitoids?

perhaps the prettiest of all found. I like the subtle banding.

Many thanks to Charley, Julia Blyth, John De Benedictus, Louie Yang, Jonah Piova-Scott and Jenn Mckenzie (who was the only one that could find occupied shelters) for help with the identification and finding of these guys.

Chenopod salt bladders

I recently published a paper on a cool plant defense system of certain plants in the Chenopodiaceae.

Three chenopod species at my field site (McLaughlin Reserve, Lake County, CA). In the center the whitish plant is Atriplex rosea, in the front and front left the dark green plant is Chenopodiastrum murale and in the back left the plant with triangular leaves is Atriplex prostrata. 

The chenopods are a diverse "family" (people can't really agree whether they are their own family or form a family with the amaranths) found worldwide. They tend to be common in three habitats, dry, salty shrublands, saltmarshes and recently disturbed areas (often roadside or agricultural). Two genera form most of the diversity and have many economically-important species in them. The first is Atriplex, the saltbushes (used to refer to perennial species) or oraches (used to refer to annual species).

A sea of Atriplex prostrata at McLaughlin. 

The second is Chenopodium, which includes the food species quinoa (C. quinoa) and lambs-quarters or pigweed (C. album).

Chenopodium neomexicanum, in the greenhouse

The coolest thing about these plants (and certain other chenopods - but not spinach or beets), in my opinion, is that they have these strange bladder cells on their leaf and stem surfaces. Several scientists have studied the salt sequestration of these bladder cells and found they are extremely important in ionic balance of the plant in saline environments. But many, if not most, of the bladdered chenopods are not halophytes (plants which live in salty areas). So what else are these good for?

The leaf of a cultivated variety of Chenopodium album. All the purple balls are salt bladders - the leaf surface below is green. 

I suspected, given their location on the plant surfaces, that they might be part of a defensive system of the plant, as they would be the first tissues contacted by herbivores and they would allow the plant to segregate defenses, which are often bad for the plant, away from photosynthetic tissues. So I tested the defensive function of these bladders by removing them from leaves and testing herbivore preference with a choice, assessing herbivore preference without a choice, and removing them in the field and assessing herbivory rates compared to control leaves.

Removed bladders from the C. album leaf above. The purple coloration is due to betalain, a compound shown in other studies of amaranths (closely related) to be an effective defense against insect herbivores. 

I found strong support for a defensive function for these structures. Plants have all sorts of cool structures (domatia, hairs, sticky glands, etc.) which are defensive in function and with this work, I added one more to this list. I'm working on a few further projects on chenopods now, I'll update with those when they get completed.

Reference: LoPresti, EL (2013) Chenopod salt bladders deter insect herbivores. Oecologia, DOI: 10.1007/s00442-013-2827-0

Fall 2013

A really busy, but awesome fall, condensed.

Spent most of my time looking at, growing, weighing, dissecting, caressing, keying, watering, fertilizing, pressing and reading/writing about chenopods.

Atriplex sp. fruiting bracts. This is probably A. rosea, though the bracts are longer and rounder than any other
A. rosea I have run into recently. 

However, I got in some wonderful camping in the mountains with friends (and the new old truck!).

Camping with the new old truck!

Where we found a few mushrooms. Some edible.

We ate chantarelles for awhile (3 meals a day for basically weeks). 

Found one lion's mane mushroom (Hericium erinaceus).

And some not:

Scaly chantarelle, Gomphus flocossus

I even took a trip home, where I learned how to differentiate the plumages of adult and 2nd winter Ring-billed Gulls (among all sorts of wonderfulness of being in New England in November and seeing family and friends). 

2nd winter Ring-billed Gull. Note the uniformly dark primaries without white spotting. Also the blueish legs and bill.

2nd winter, in front, with two adults, behind. 

I'm about to depart on all sorts of adventures (Bahamas! Jordan and Israel!), I'll update this again at some
point.

Bodega Tropical Kingbirds

After a maddening seawatch for boobies at Bodega Head, Jay Riggio, Jessie Godfray and I went down a little bit looking for migrant passerines at a nearby small pond (with the clever name: hole in the head). After quickly hearing a kingbird, we located it briefly and saw that it was quite a yellow bird. I immediately called it a Tropical and then spent the better part of a half hour while we tried to relocate it convincing myself that it couldn't have been one. Luckily, Jay had more faith and after a bit of looking, we relocated it and saw the key fieldmarks: the extensive yellow, lack of white outer rectrices on a brown - not black - tail with a notch.

Yellow, yellow and more yellow. Also the massive bill. 

notched tail, check. no white rex, check. 

At the same time we were watching one bird and noting these characteristics, another one called. Tropicals sound harsher and quicker to me than Western (or Eastern, for that matter). Eventually we saw both at once.

The last time I saw Tropical Kingbird was May of 2012... been out of Latin America for too long. I can't find a picture of a Tropical Kingbird from any of my travels, though they were common birds in Argentina, Uruguay and Peru. So instead, here is my favorite kingbird:

Snowy-throated Kingbird, Bosque de Pomac, Lambayeque, Peru. April 2, 2011

Shelter-building caterpillars

This post is a bit late in coming, but I wanted to share what I worked on for several summers with Doug Morse for my undergrad thesis. We did most of the work in 2008 and 2009, but finished up some during the summer of 2012 and it was published earlier this year.

Caterpillars, like many other animals, construct shelters for themselves, by some estimates over 60% of lepidoptera (butterfly and moth) species make some sort of shelter. Most often these are made by folding or rolling the leaves which they feed on into shelters. The shelters likely serve a variety of purposes: protection from dessication, protection from predators, reduced probability of dislodgement, etc. Interestingly, several studies had found that caterpillars in shelters suffered less predation but more parasitism and indeed, at least one author had speculated that since parasitism was often so high (90%+ sometimes!), that shelters must not be good protection.

an unidentified caterpillar folding up a Malvaceae leaf, Chiloe Island, Chile

That seemed odd to me; if parasitism was so prevalent, it must be a strong selective force and clearly some survive, so there must be some way to beat it. Working with a cool leaf-rolling moth, Herpetogramma thesausalis, on ferns in Maine, I ran experiments to test two hypotheses:

1) Shelters provide protection from parasitoids
2) Shelters are costly for the caterpillars to produce

an adult male H. thesausalis on sensitive fern, its primary host

To test the first hypothesis, I thinned shelters during the moth's pupal stage by carefully removing the outer layer of fern (the shelters usually involve 2-4 layers, so this did not expose the pupae inside). I used the pupal stage, as caterpillars would quickly rebuild the shelter when I thinned it - pupae are unable to. I found that parasitism almost doubled without that outer layer, though overall size of the shelter was only slightly smaller. Therefore, I found support for the first hypothesis - the first experimental evidence for this function of caterpillar shelters!

A cross-section of a shelter containing a parasitoid (Alabagrus texanus) cocoon.

For the second hypothesis, I divided caterpillars on ferns into three groups: the first I left alone (as controls), the second I dismantled their shelter every few days and the thirds I touched but did not destroy the shelters at the same interval. In essence, I was forcing one group to remake their shelters. Given my hypothesis, I expected that these caterpillars would either pupate smaller or later. Interestingly, the caterpillars delayed their pupation in order to rebuild shelters - an average of ~2 days later than the other groups - and they did not eclose smaller (or build smaller shelters!). Delaying their pupation puts them at increased risk for larval parasitism and delays their reproduction (the population is fairly synchronous, so this could be a big cost for some individuals). Hypothesis 2 supported!

A female ichneumonid (Itoplectis?) oviposits into a caterpillar shelter.

There is more to the story, it is a longer paper. But perhaps the most interesting thing is that there are two broad guilds of pupal parasitoids - those with long ovipositors (as seen in the above picture), which oviposit from outside the shelter, and those with short ovipositors which gnaw their way through the seams between leaves into the shelters. I suspect that larger shelters, with a longer distance between the outside and the pupa, are better protection against the former guild. However, in a larger shelter, there are more seams, which may make it easier for the latter guild to parasitize, an interesting trade-off, which I have only observational data to support.

Phaeogenes hebrus, the most common short-ovipositor species in this system.

The paper can be found here: http://link.springer.com/article/10.1007/s11829-013-9261-4#page-1 . Arthropod-plant interactions publishes lots of great - if limited interest - research, I read a very high number of the papers it publishes.

This would make a cool tattoo, eh?

More on parasitoid nuptial gifts

I did a bit more poking around the literature (there is, fortunately, quite a lot on parasitoids) and found many other examples where some comparison was made between mated and virgin females. Every paper seemed to have different methodology and different measured metrics (related to whatever the paper was about).

A bad picture of a beautiful wasp, Mesostenus thoracicus, female, Walpole, Maine, 2009

The results of all these studies were not at all in agreemend. Some agreed with the findings in Bracon hancocki and found that virgins lived significantly shorter lives than mated females. Others found the exact opposite. Many showed that virgins lay fewer eggs or parasitize fewer hosts (independent of eggs, as in many cases more males can develop in a host than females), but others found the opposite result. Some showed that virgin females spent less time moving and ovipositing than mated females, which suggests they wait for mates. Others found no difference in similar metrics.

An unidentified Ichneumonid (Pimplinae?) ovipositing into a Herpetogramma thesausalis pupa, Maine, 2009

Perhaps the most interesting result was that of Sagarra et al (2002) who found that female Anagyrus kamali did not differ in longevity based on mating status, but males did. Unmated males lived 40% longer than mated males and females required more than one mating to get sufficient sperm to fertilize all their eggs (some scientists believe this is rare in parasitoids, others don't - I don't have an opinion). This does suggest that males put some serious investment into their sperm, as all other conditions were equal for these males.

Bob Carlson, one of the most knowledgeable Ichneumonid specialists around, said: "There are so many kinds of parasitoid Hymenoptera, that I expect it certain that some of them have evolved such that females get sustenance from male seminal fluid. "

That seems pretty reasonable to me, though it might be a needle in a haystack search for it. Anyone interested in the references I have compiled on this or a longer summary of each paper's finding, let me know. 

This Ichneumon (Ichneumoninae, I believe) is a rare parasitoid of  Herpetogramma thesausalis. This male was
buzzing around a patch of sensitive fern with lots of host shelters, likely mate-searching.

Parasitoid nuptial gifts?

A Braconid, Alabagrus texanus, a male. I doubt any nuptial gifts are given in this species scramble-mating system. 

I found something yesterday that I think is really-cool. While browsing old copies of the journal Bulletin of Entomological Research, I stumbled across this quote, in reference to Bracon sp. (probably hancocki).

"Average life-span for mated females was 13.6 days, whereas virgin females lived for an average of 5.6 days."

Here's the catch: parasitoids are unreported (at least that I could find) to give "nuptial gifts" i.e. a resource given by male to female during courtship or copulation. Charles Godfray, in his book (bible), Parasitoids: Behavioral and Evolutionary Ecology, says "I know of no evidence of nutrient transfer during mating in parasitoids". Many other insects are known to (katydids, certain flies, etc.). This quote makes it seem like there could be some transfer of nutrients in the sperm (as the authors made no mention of courtship behavior).

Making the story more interesting, and believable, the authors state that the females copulated many times with the same male upon emergence, then began egg-laying a few days later. Multiple matings are rare in parasitoids, another indication that the female is likely gaining something else besides just sperm from the male.

An interesting observation, and one that probably could be examined, as Bracon is a fairly common genus.

Reference: Olaifa, J. I., & Akingbohungbe, A. E. (1982). Bionomics of Bracon ?hancocki (Wilkinson)(Hymenoptera: Braconidae), a Larval Parasite of Cydia Ptychora (Meyrick)(Lepidoptera: Tortricidae) in Nigeria. Bulletin of Entomological Research, 72(04), 567-572.

Godfray, HC. (1994) Parasitoids: Behavioral and evolutionary ecology. Princeton University Press. 

This is the same species in the photo above emerging from a Herpetogramma caterpillar, prior
to spinning its cocoon.