Holiday caterpillar cookie!

I don't think this one is aposematic!

I may be the only one to have ever received an eyespot caterpillar cookie.

Cookie credit: Holly K.

The Puss Moth (Cerura vinula) - (Family: Notodontidae)

The Puss Moth (Cerura vinula) - Family: Notodontidae

As a reminder, my project involves the examination of the evolution and function of caterpillar eyespots. Throughout my blog you can now find a few great examples of the kinds of caterpillars I am talking about (e.g., Therinia transversaria, Xylophanes germen, Prepona sp.). For many of these, it seems fairly obvious that the eyespots are mimicking the eyes of a snake or other predator. However, we should not immediately discount other possible functions of caterpillar eyespots. Take the Puss Moth caterpillar for example:

Like most eyespot caterpillars this caterpillar initially relies on crypsis via protective coloration. Here is the caterpillar at rest on its food plant:

Once detected or harassed the caterpillar reveals a pair of black spots and directs them towards the threat:

...and once again we meet a species where the beauty of the caterpillar far outmatches that of the relatively drab adult life stage:

The defensive behaviour of the Puss Moth caterpillar is incredibly interesting as well and is described by E. B. Poulton in his classic book "The Colous of Animals". Below is his description and inferences on the defensive behaviour of the Puss Moth caterpillar:

"The same larva assumes a terrifying attitude (mimetic of a vertebrate appearance) when disturbed"

As soon as a large larva is discovered and disturbed it withdraws its head into the first body-ring, inflating the margin, which is of a bright red colour. There are two intensely black spots on this margin in the appropriate position for eyes, and the whole appearance is that of a large flat face extending to the outer edge of the red margin (see fig. 60). The effect "is an intensely exaggerated caricature of a vertebrate face, which is probably alarming to the vertebrate enemies of the caterpillar. The terrifying effect is therefore mimetic. The movements entirely depend on tactile impressions : when touched ever so lightly a healthy larva immediately assumes the terrifying attitude, and turns so as to present its full face towards the enemy ; if touched on the other side or on the back it instantly turns its face in the appropriate direction. "

Unlike Poulton, I am not fully convinced that because the caterpillar has a pair of spots that may vaguely resemble a vertebrate face (to us) that the "terrifying effect is therefore mimetic". The important question really is whether the black spots sufficiently resemble the eyes of a predator for this caterpillar to gain protection (via mimicry) from an attacking bird.

Poulton's description of the caterpillar continues:

"Effect heightened by two pink whips"

The effect is also greatly strengthened by two pink whips which are swiftly protruded from the prongs of the fork in which the body terminates (see fig. 61). These prongs represent the 1st pair of larval legs, which have been greatly modified from their ordinary shape and use. The end of the body is at the same time curved forward over the back (generally much farther than in fig. 60), so that the pink filaments are brandished above the head. Although the filaments are no thicker than a rather coarse cotton thread, they are hollow, and contain a delicate muscle which runs through their whole length and is attached at the top. When the muscle contracts the filament is withdrawn, being turned outside in : protrusion is brought about by the pressure of the blood, which drives the filament before it. ...The appearance of the caterpillar is sufficiently alarming to human beings, and most people believe that the black marks are really eyes. Eosel was afraid to touch the larva when it assumed its terrifying attitude. Izaak Walton speaks of the black marks as ' his eyes black as jet,' in a description ..."

"The larva of Puss Moth can further defend itself by ejecting an irritant fluid"

All the defensive measures hitherto described are of a passive nature, but if further attacked the caterpillar can defend itself in a very effective manner. The lower part of the red margin below the real head of the animal is perforated by a slit-like opening (see fig. 60), leading into a gland which secretes a clear fluid. This fluid is stored up in considerable quantity and is ejected with great force when the caterpillar is irritated. The ' face' being turned towards any point at which the larva is touched, the stream is sent in the direction of the enemy. It has been long known that this fluid causes acute pain if it enters the eye. ... The secretion proved to be a mixture of formic acid and water : in a mature larva the proportion of acid is as high as forty per cent., and a twentieth of a gramme can be ejected if the caterpillar has not been irritated for some days. Half grown individuals eject nearly as much, but the fluid is weaker, containing about thirty-three to thirty-five per cent, of acid. ... So far as we know at present, no other animal secretes a fluid containing anything which approaches this percentage of strong acid.

The value of this strongly irritant liquid is sufficiently obvious. I have seen a marmoset and a lizard affected by it, and have myself twice experienced sharp pain as the result of receiving a very small quantity in the eye. Although the secretion is therefore useful as a defence against vertebrate enemies, it is probably chiefly directed against ichneumons."

When reading this account I began to wonder whether the black spots are really a poor mimic of predator eyes, or instead they - along with the pink whips - are part of a warning to attackers that the caterpillar has a formic acid spray. The "pairedness" of these spots could simply be a result of bilateral symmetry, and paired objects are likely to be more conspicuous to the vertebrate eye possibly enhancing the conspicuousness of a signal (Stevens 2005). For this species which possesses an effective chemical defence, it seems more likely to me that these spots form a part of a conspicuous warning signal which lets the attacker know that the caterpillar is chemically loaded.

Let me know what you think, click the link and add a comment below.

Aside: Interestingly, there are several other species of insects that use formic acid to defend themselves from attackers. The carabid beetle Galerita lecontei has the highest concentration of formic acid that I have seen reported (80%). This species can also aim its spray accurately towards attackers. See a full account of the chemical defence of Galerita lecontei here. Camponotus floridanus ants can also aim and spray formic acid on attackers.

Update: Here is a video showing late instar caterpillars and the adult: 

Caterpillar of the day: Therinia transversaria

It has been a while since I have had a solid post dedicated to caterpillar eyespots. I have now returned from by research trip to Costa Rica, but I will try to keep sharing its beautiful diversity through the photos and videos that I captured while I was there. The last caterpillar I observed on my final official day of caterpillar data collection was quite an exciting specimen. I was particularly excited because this caterpillar exhibited some interesting body posture changes upon my simulated attacks (i.e., light pinching with forceps).

Therinia transversaria (Saturniidae)

The photo above shows the typical resting position of this caterpillar (at least in this instar). Very cryptic, with dashes of brown that cross the body and break up its outline - a strategy known as "disruptive colouration". Note also that the caterpillar folds its body in such a way that the brown on the anterior end seems to line up with the brown on the central part of the body. This seems to be a good example of a special form of disruptive colouration termed "coincident disruptive colouration" where crypsis is increased through preventing detection of revealing body parts by visually joining them with other parts of the animal's body.

Interestingly, similar colour patterns in caterpillars caught the attention of Edward Bagnall Poulton who was one of the early evolutionary biologists / naturalists to take a close look at animal coulouration and ponder its function. His book "The colours of animals: their meaning and use, especially considered in the case of insects" published in 1890 remains a highly regarded (and cited) work on animal colour patterns and their function. For a great synthesis on disruptive coloutarion and its various functions see Martin Stevens and Sami Merilaita's recent paper on the subject:

Stevens, M. and Merilaita, S. (2009) Defining disruptive coloration and distinguishing its functions.Philos Trans R Soc Lond B Biol Sci. 364: 481-488

Once the caterpillar realizes that it has been discovered it reveals its previously hidden eyespots:

When attacked, the caterpillar pulls in its head and puffs out the body segments that have eyespots:

This is very similar to the behavour I observed in Papilio canadensis caterpillars upon attack and the behaviour apparently observed in many caterpillars with eyespots, including Sphingidae caterpillars from the genus Xylophanes  (e.g. X. tersa).

A Saturniidae bee mimic?

More Saturniidae moths were posed around my light tonight and one looked to be a different species within the genus Automeris. I poked it to see if its eyespot display differed from the other Automeris species I have seen (and poked). To my surprise it didn't reveal eyespots, nor did it fly away. Instead, it raised its wings up behind its back and fully displayed its yellow body with a black stripe. See photos below:

Before:

Post-poke:

To me it [vaguely] resembles a bumble bee. I have never heard of this behaviour or defensive strategy in Saturniidae moths, but it is incredibly interesting. Bees are common models in mimicry systems - especially in mimetic flies (e.g. Syriphidae). By resembling bees or wasps (sometimes relatively poorly) mimetic flies avoid persecution by birds so there is no reason to think that a similar strategy wouldn't work for these moths. Please leave a comment if you have any information about this species or thoughts of the defense mechanism !

I didn't get a look to see if it also has eyespots hidden in the wings. This would be interesting to know, because so many Saturniidae moths have eyespots. It is possible that this one does too and just doesn't use them. It would be interesting to know whether this species evolved from an ancestor that used the eyespot-defence. IF so then it raises some interesting questions:

· What conditions made individuals with the bee mimic defence better than ancestors with eyespots?

· Why don't more Saturniidae moths use a similar defence?

Heliconious PWND!!!!!!!!1

During my time here in Costa Rica I have slowly come to love the butterflies from the genus Heliconius. Quite a beautiful genus with distinct elongate wings that are black and marked with a splash of orange, pink or blue. Their colour pattern is a signal to bird predators that they are unpalatable. In some species this is an honest signal indicating that the butterfly is truly unpalatable, but other species are mimics. Henry Walter Bates was very interested in Heliconidae butterflies. In his book The Naturalist on the River Amazons he discusses Heliconius butterflies at some length (click here to have a read). Also, Bates' classic manuscript was focused on Heliconidae: Contributions to an insect fauna of the Amazon Valley : Lepidoptera : Heliconidae.

Today while searching for caterpillars I found a spider nomming a Heliconius genus butterfly. The spider was surprisingly small to have taken down such a large prey item. Not sure yet on the species involved and suggestions are welcome! Here are some photos of the action:

Heliconius sp. (Nymphalidae) caught by a spider

I'm not yet sure whether this Heliconius is an aposematic or mimetic species. I suspect that the chemical defence (and colourful warning signals) of Heliconius are directed towards birds, so for this spider it probably doesn't matter either way. It seems many insect species that are unpalatable to birds are fully palatable to invertebrate predators.

Eyespots and the amazing Macrocilix maia

I am continually astonished by anti-predator defences in insects. One day it might be an insect that is so well camouflaged that you struggle to find only even when you are literally inches away. The next day it could be an astonishing mimic like a fly that mimics a bumble bee. Of course eyespots have their own appeal; conspicuous circular markings that resemble eyes, usually in direct contrast with the rest of the animal's body which is amazingly well camouflaged. Eyespots with an anti-predator function have been described in fish, birds, amphibians, and of course insects. Some of the best known examples come from Lepidoptera (butterflies & moths).

Today I found some beautiful adult moths from the genus Automeris (Saturniidae). When threatened they have the interesting behaviour of spreading their forewings and revealing otherwise-hidden eyespots. To get a sense of what this behaviour I gently prodded a few. The moths spread their wings and showed off their eyespots, sometimes in doing so they fell to the ground. Even as they fell, and upon landing, they held those wings open. After roughly 2-3 minutes the wings slowly returned to their natural "tent" resting position. Subsequent prods sometimes would elicit the behaviour again, but usually initiated an escape flight response instead. This is what they look like:

Recently there has been discussion over a new and unique type of colouration on the wings of an adult Lepidopteran. The descriptions of this species from Boneo and Malaysia are borderline unbelievable.  I have to say that I was skeptical (to say the least) when I heard the descriptions. If you look hard enough at something you can often see amazing things that arn't really there.

Without tainting your view by telling you what other people see have a look at some of these photos of the moth Macrocilix maia:

 http://www.flickr.com/photos/allanlee/3506113435/

http://www.flickr.com/search/?q=macrocilix+maia&w=all&s=int&referer_searched=1

When you see the photo it really is amazing. The accompanying descriptions are just as interesting. Right now there is rampant speculation on exactly what these colour patterns are supposed to resemble. Jerry Coyne has a great blog post on it here. Read the comments below his post to see some interesting ideas.

Some are suggesting that it could be a phenomenon new to biology: mimicry of an entire scene. Currently, my view is that this is a form of masquerade: a moth that with descrete, high-contrasting markings that seem to vaguely resemble flies buzzing around a piece of feces/rotting flesh. This probably protects the moth by causing the predator to misclassify it as an inedible object(s). It seems possible that a predator big enough not to be interested in eating little flies should pass over it, but anything small enough to want a fly might not be able to subdue a big moth.

Some preliminary questions are left in my mind though:

• Wouldn't this moth have to rest on a white background for this to work, and where are these white backgrounds?
• There are flies and discrete piles of decaying crap elsewhere, why don't we see similar adaptations elsewhere?
• Does the moth move its wings to simulate buzzing flies?

As always, your thoughts and comments are welcome below, just click the "comments" link below this (or any other) post to leave a message.

Caterpillar of the day: Xylophanes [germen?]

In the Cacao Sector of the ACG today I finally saw my first early-instar Xylophanes sp. caterpillar (I think Xylophanes germen). Green with mostly yellow eyespots! I hope to see more, but apparently they are more frequently observed here in May and June. One of the parataxonomists at Cacao told me that there are roughly 7-8 species of Xylophanes in the Cacao Sector alone!

Xylophanes sp. (Sphingidae)

I was excited to see yet another bag labelled "Sphingidae", but unfortunately for me (and the caterpillar) it had been parasitized:

You can even see the classic Sphingidae 'horn' in what is left of the deflated caterpillar body. An even better photo is below. This is a parasitized Xylophanes cthulhu caterpillar that I came across on the ACG caterpillar database - you can even see the eyespots still!

It almost looks like the paracitoid cocoon is dressed as a ghost for Halloween doesn't it? If the caterpillar that I observed today really is Xylophanes germen, it would be great to see this guy in its later instars - they are pretty intense.

Xylophanes germen (Sphingidae)

Photos below from the ACG caterpillar database

Ultimate instar:

[relatively drab] Adult:

Caterpillar of the Day: Neococytius [cluentius?]

This caterpillar was observed at the San Gerardo Station in the ACG. I saw this individual twice, so I have photos from both the pre-penultimate and ultimate instars. Another giant Sphingidae. This specimen thrashed its anterior half quite violently when it was pinched with forceps (especially on Aug 26). In the late instars these guys get to be >100 mm long.

Neococytius [cluentius?] (Sphingidae) Aug 15 2011 - Pre-penultimate instar

Neococytius [cluentius?] (Sphingidae) Aug 26 2011 - Ultimate instar

Neococytius [cluentius?] (Sphingidae) Aug 26 2011 - Ultimate instar 

Neococytius [cluentius?] (Sphingidae) Aug 26 2011 - Ultimate instar 

It seems like the white could make these guys blend in to the foliage by resembling the streaks of sunlight that pass through the canopy. Many predators use edge detection to recognise prey items, so this colour pattern could also help break up the outline of the caterpillar when it is sitting on a leaf.

The pupa is a typical looking for a Sphingidae (photo from the ACG database):

This caterpillar will eventually grow up to look like this (photo from Wikipedia.org):

Just another great example of a species where the caterpillar is more beautiful than the adult!

Continuing on the theme of masquerade...

As promised here are some photos of that caterpillar that was peeking out in one of the photos in my last post. This is another Prepona sp. but I'm not sure which. I only found it because of the conspicuous frass pile collecting on a leaf underneath. What drew me to that tree though was the characteristic feeding damage from Prepona caterpillars. They chew off the first half of the leaf but leave the middle vein, then to that vein they silk small cut trimmings of that leaf to give it a "trashy" kind of look. During the smaller instars the caterpillars are usually seen dangling from the end of the vein in full sight, but they look so much like the other "trash" that you often miss them. The bigger ones will sit right on top of leaves or on branches. This one was dangling from a full dead leaf that had been silked to the branch. It was wrapped kind of in a spiral shape on that handing leaf. I showed it to several people and they didn’t see it even when they were inches away.

Prepona sp. (Nymphalidae)

Here is a smaller individual from the same plant (maybe a full sib). The first photo below shows the characteristic feeding damage.

It almost disappears once it gets amongst its "trash" on the leaf vein. In many ways masquerade is more similar to mimicry than crypsis. When people discuss crypsis as an anti-predator defence they usually mean that the predator does not detect the prey. It is perhaps more realistic to recognise that the predator does see the object it just doesn't think that that object is a meal. In classical Batesian mimicry theory, the number of mimics should be smaller than the number of models (model = the object being mimicked), otherwise predators don’t learn to avoid that type of prey. Biologists call this "frequency-dependence" because the efficacy of the defence depends on the relative frequency of the models to mimics. In theory this should be the case in masquerade too, it's just that the model is usually something incredibly common like a living/dead leaf or a twig.

On a night walk tonight I found another dead leaf mimic:

A colleague/friend recently blogged about The weird and wonderful world of katydids. I doubt that I could do a better job of enthusiastically describing these guys so I'll leave you to read his post. He writes very well and I highly recommend following his blog: Katatrepsis. He's right though, the detail of the false venation is mind-blowing.

Non-caterpillars and coincidental eyespots

I set out today looking for caterpillars in the forest here in Santa Rosa (ACG). Finding caterpillars is no easy task, but can be fun and very rewarding when you do have a good find. Caterpillars get hammered by predators so it pays to be highly cryptic. Even when you know where and when to look, it can be very difficult. The parataxonomists in the park here consistently blow people like myself away with their trained eyes scanning the foliage.

Many caterpillars employ a "masquerade" strategy, looking like various inedible items in their habitats. Here in the tropics dead leaves are a common model. To give you a sense of why this might is the case, here are a set of caterpillar-like objects that I saw today in the forest.

One of the above photos actually does have a caterpillar hiding in it. Scroll up and see if you can find it!

Hint: the caterpillar’s frass (caterpillar poo) gives it away.

You can see the little head peeking out from the top right of the hanging dead leaf in the last photo. Actually, I found 3 different individuals on the same plant, presumably all the same species of the Prepona genus (Nymphalidae). I think these are a different species from the 2 other Prepona species I have encountered here at the ACG. I will post some shots of these new guys tomorrow.

Another thing that I observed was several paired circles in the forest that were totally innocuous. Here are a few examples:

OK, I'll admit that it is a bit of a stretch to say those look like eyes. The point I'm trying to make is that there are (implicitly) other cues involved. One of the arguments used to support the idea that eyespots are mimicking eyes is that when animals see objects that even vaguely look like eyes it usually indicates a threat. Immediate retreat from anything that looks remotely eye-like should be a must for these attackers (e.g., small birds), or else they risk death (e.g., an attack from a snake). But fleeing from everything that looks remotely eye-like must also entail a cost, either energetic (quick retreat should have some energetic cost) or opportunistic (missing out on a big meal). Obviously other cues in addition to the eyespots are critical to initiate a retreat from an attacker; things like hostile behaviour that resembles an attacking or dangerous snake.