Defensive Posture & Eyespots Protect Caterpillars

Pastry "caterpillar" used to examine the protective effect of eyespots and defensive posture of caterpillars.

You may recall that Tom Sherratt and I published a paper last year in Animal Behaviour on the protective value of eyespots to model caterpillar (see more about this work here). In this paper we found that eyespots could protect prey, but the protective effect was dependent on other aspects of caterpillar body colour. Specifically, the protection conferred by eyespots was less when caterpillars were a uniform green than when those caterpillars were two-toned (i.e., countershaded). Overall the protective effect of eyespots was much weaker than we had anticipated, perhaps because our pastry caterpillars don't exhibit any of the behaviours that real caterpillars do when they are attacked by birds. This led us to consider another feature of these caterpillars that may augment the protective effect of eyespots - their defensive posture.

The vast majority of the caterpillars with eyespots that I have had a chance to examine have some form of defensive posturing upon perceiving a threat. Some species tuck their head under their body and puff up their thoracic body segments (e.g., Papilio canadensis, Papilio troilus), while others pull their head telescopically into their body which also puffs up their thoracic segments (e.g., Xylophanes sp.). The suggestion has been that this defensive posture augments the protective effect of eyespots.

Papilio canadensis caterpillar on a branch in its defensive posture.
This is my photo of a caterpillar that I reared for another project.

Xylophantes juanita (Sphingidae) caterpillar in defensive posture.
Photo from Janzen & Hallwachs database.

There are a few reasons why the defensive posture might increase the protective effect of eyespots. First, it could help emphasize the markings to an attacker by drawing attention or emboldening the spots. Second, it may help the caterpillar appearing larger enabling it to buff predators away from attack. Finally, this posture might make the anterior body segments resemble the head, perhaps increasing overall resemblance to a snake by placing the false eyes (i.e., eyespots) in the context of a "head". Interestingly, several caterpillars engage in a similar defensive posture, including some with poorly developed eyespots or where eyespots are lacking altogether. Thus "head-shape" might be a mimetic signal in and of itself. Our goal was to test whether eyespots and the defensive posture protect caterpillars from birds, and if so, does having both traits increase protection even more?

Materials & Methods

It wasn't possible to deploy real caterpillars in the field, so we used artificial caterpillars made of flour and lard. We had observed previously that eyespots were more effective when the caterpillars were two-toned (i.e., countershaded), so we made all our prey two-toned by combining dark and light green dough (dyed with food colouring). All caterpillars were formed into 4 cm long cylinders, then to make the "defensive posture" prey we pressed these half of these caterpillars into a mould made from plaster of Paris. This ensured that all model prey (rest or defensive posture) the same volume, just like a real caterpillar that has shifted its posture.

Preparing to make the mould for this experiment

The finished mould. It cracked in half when I was removing it.

Over the course of a summer we made and deployed 576 model caterpillars, divided evenly among four treatments:

1. No eyespots - Resting posture
2. Eyespots - Resting posture
3. No eyespots - Defensive posture
4. Eyespots - Defensive posture

No eyespot - Resting posture treatment

No eyespot - Defensive posture treatment

Eyespot - Defensive posture (above) and Eyespots - Resting posture (below) treatments.

Model prey were deployed in the field by pinning them to tree branches. Each tree had four caterpillars - one of each treatment. We deployed caterpillars 6 times (i.e., 96 prey deployed each time), always in a new location, then tracked their survival three times a day over the next 90 h. Sometimes prey were gone, other times they were riddled with peck marks. Here are some examples of pecked "caterpillars" from the field:

Results & Interpretation

Our results showed that both the defensive posture and eyespots reduced the number of attacks, but having both traits didn't further increase the protection. This was surprisingly consistent with another recent study that examined rates of predation on model snakes with a viper-like head shape and/or zigzag patterning (Valkonen et al. 2011). They too found that possessing either trait conferred protection, but having both traits didn't increase that protection further. This seems to make sense - if either trait indicates risk from a threat, having both traits may help better identify that threat but doesn't change the risk associated with it. It is still unclear though how predators decide which cues reliably indicate a threat and which do not. A better understanding of this learning process might also help us understand why so many mimics only vaguely resemble their model.

Figure 2 from Valkonen et al 2011 showing number of raptor attacks on snake replicas

See the full Valkonen et al 2011 paper for free here:

Valkonen JK, Nokelainen O, Mappes J (2011) Antipredatory Function of Head Shape for Vipers and Their Mimics. PLoS ONE 6(7): e22272. doi:10.1371/journal.pone.0022272

We also looked at the number of pecks per caterpillar as well as where they were pecked. Caterpillars with both eyespots and the enlarged "head" shape received more "head"-directed pecks that caterpillars with either trait alone. Assuming birds direct their attacks toward a prey or predator's head, this might mean that birds still do perceive the anterior segments as more head-like when they have both traits - just not enough to deter their attack/curiosity.   

The next step for this research is to see if we can determine why the wide "head" defensive posture works. Of course the leading hypothesis is that this posture makes the caterpillar look more snake-like, or perhaps more like a viper. To make this argument convincingly you would need to show that these caterpillars look more like snakes (or perhaps vipers specifically) when they are in their defensive posture compared to when they are at rest. We are currently working on a project that examines whether or not this is the case using photos of preserved snakes and live caterpillars.

References:

Hossie, T. J., Sherratt, T. N. (2012) Eyespots interact with body colour to protect caterpillar-like prey from avian predators. Animal Behaviour 84(1): 167-173, doi:10.1016/j.anbehav.2012.04.027

Hossie, T. J., Sherratt, T. N. (2013) Defensive posture and eyespots deter avian predators from attacking caterpillar models. Animal Behaviour [Early View]

Eumorpha labruscae: another caterpillar with a blinking eyespot

Eumorpha labrusace (Sphingidae)

Eumorpha labruscase caterpillar, penultimate instar. Closely related to Eumorpha phobas.
Note the red anal horn which can be moved actively when the caterpillar feels threatened.
Photo from Janzen and Hallwachs' database.

Continuing on a theme, here we have another spectacular caterpillar - Eumorpha labruscae. This species is more common than its close relative E. phorbas, and is found in both dry forest and rainforest habitats. Even this species however is still only infrequently observed as a caterpillar. Like E. phorbas this caterpillar will gain a "blinking" eyespot in its ultimate instar. See also my earlier posts about blinking eyespots here and here.

Early Instars:

The specimen in the photo at the top has not yet reached its final instar where it will gain the blinking eyespot. Instead, it has a long red anal horn that it can flick or whip back and forth. The anal horn is actually soft and harmless, its purpose is probably to intimidate or bluff predators away from attack. While it is waving this horn the caterpillar simultaneously pulls its head into its body telescopically. This widens its anterior body segments which have false eyes (eyespots) and creates the overall impression of a snake's head. I have embedded a short video clip of the defensive display below:

I have never seen a specimen in an earlier instar than this (i.e. a pre-penulitimate instar caterpillar), not even a photo of one. I would guess that they looks similar to the the early instars of Eumorpha phorbas (see them here). A note from the database record for the specimen at the top states that the "...PPU instar looks like normal Eumorpha satellitia..."

Ultimate instar:

Yes, the caterpillar is quite impressive in the early instar depicted above, but the final caterpillar instar of this caterpillar is equally impressive. The specimen at the top is the same specimen depicted below. It was found after a tree fall in 1978 feeding on a woody vine (Cissus alata). As with E. phorbas, feeding on these canopy-level vines may help explain why these caterpillars are observed so infrequently. Other specimens have been found feeding on C. biformifolia, C. fuliginea and C. verticillata. Apparently the caterpillars also feed on another closely related group of vines in the genus Vitis, including the species Vitis labruscae where the species name may haveprobably come from. The caterpillars get quite large by this stage reaching sizes around 80 mm.

Eumorpha labruscae caterpillar, ultimate instar. Costa Rica. Caterpillar is in its defensive posture.
Photo from Janzen and Hallwachs database.

As you can see, the caterpillar keeps many of their snake-like characteristics from the earlier, like the eyespots on the body segments near the caterpillars real head. Even when walking around this caterpillar appears to be a pretty convincing snake mimic (at least to human eyes). It also sheds the long red anal horn, which is now replaced by a shiny black spot that it can actively move. Here is a closer look at the posterior "blinking" eyespot of Eumorpha labruscae:

Posterior "blinking" eyespot of Eumorpha labruscae caterpillar, ultimate instar. Costa Rica.Photo from Janzen and Hallwachs database.

By moving this black spot on its posterior (rear) end the eyespot appears as though it were a blinking eye. The caterpillar actively "blinks" this eyespot when threatened, and we think that this "blinking" eyespot is meant to scare off attackers. Interestingly though, snakes don't have eyelids (they have transparent eye scales called brilles instead) and therefore do not blink! So then what is this "blinking" eyespot mimicking? We suspect that it is perceived by predators as a blinking eye of some other vertebrate, perhaps the eye of a lizard, mammal, or bird that does blink. It could be that the caterpillar mimics a snake from the anterior end, and by mimicking a different kind of eye at the posterior end the caterpillar increases the range of predators that it is protected from. As I have mentioned these caterpillars are only rarely encountered, so unfortunately this means we have not yet had a chance to determine how the relevant predators react to the "blinking" eyespot.

I have embedded two great videos of the ultimate instar caterpillar in action. The first clip shows off the anterior eyespots and the snake-like head, and the second one shows the blinking eyespot really well:

Adult:

The adult life stage of this species is actually quite handsome. Their wingspan ranges from at least from 85-115 mm. The colour of the underwings is presumable where the species gets its common name - the Gaudy Sphinx. The species occurs throughout Central America, but also extends northward through the United states (sometimes up to Saskatchewan and Manitoba, Canada), and southward occasionally as far as Argentina.

Eumorpha labruscae adult male. Cost Rica. Wingspan: 111 mm
Photo from Janzen and Hallwachs database.

Eumorpha labruscae adult male. Cost Rica. Wingspan: 115 mm
Photo from Janzen and Hallwachs database.

Find out more about "blinking" eyespots or Eumorpha labruscae by following the links below:

• An eyespot that blinks?
• Eumorpha phorbas: a caterpillar with a blinking eyespot
• Silkmoths - Bill Oehlke - Eumorpha labruscae
• CATE Sphingidae - Eumorpha labruscae

A more complete description of the "blinking" eyespot in Eumorpha labruscae and its close relative E. phorbas as well as our thoughts on this eyespot's possible function in deterring predators can be found in our recent manuscript published in the Journal of Natural History:

Hossie, T.J., Sherratt, T.N., Janzen, D.H., Hallwachs, W. (2013) An eyespot that “blinks”: an open and shut case of eye mimicry in Eumorpha caterpillars (Lepidoptera: Sphingidae). Journal of Natural History DOI:10.1080/00222933.2013.791935

Eumorpha phorbas: a caterpillar with a blinking eyespot

Eumorpha phorbas (Sphingidae)

Dorsal view of Eumorpha phorbas caterpillar, final instar. Photographed during my 2011 trip to Costa Rica.

 Above is a photo of the caterpillar as I observed it - a final instar larva about 60 mm long and 12 mm in diameter in the middle of the body. This specimen had been collected by parataxonomists in an earlier instar while feeding on Sarcopera sessiliflora (Marcgraviaceae). Eumorpha phorbas caterpillars are only encountered on very rare occasions - I just happened to be fortunate enough to be visiting the research station in Costa Rica as the caterpillar reached this final instar. This species is restricted to rain forest habitat and its host plant (Sarcopera sessiliflora) is a canopy-level large woody vine. A preference for this canopy-level host plant partially explains why the caterpillar is observed so infrequently. This one had been discovered by parataxonomists upon searching a 25 m tall tree had been uprooted.

Click here to find out more about parataxonomists and their role in setting up tropical biodiversity for conservation through non-damaging use!

Early Instars:

During the earlier instars these caterpillars rely largely on colour-matching the green leaves of their host plant Sarcopera sessiliflora. You will notice however that the caterpillar has a bright marking on the thoracic body segments, what we would consider a weakly-developed eyespot. It is unclear whether these markings provide much protection to these early-instar caterpillars. We aren't even sure if the marking indicate the beginning of eyespots evolving in this species or the reduction of conspicuous marking as they are being selected against. We do know however that a closely related species, Eumorpha labruscae, has well developed eyespots even in these earlier instars.

Eumorpha phorbas caterpillar, pre-penultimate instar. Costa Rica.
Photo from Janzen and Hallwachs database.

Eumorpha phorbas, pre-penultimate (3rd) instar. Costa Rica.
Photo from Janzen and Hallwachs' database.

Dorsal view of Eumorpha phorbas, penultimate instar. Costa Rica
Photo from Janzen and Hallwachs' database.

In the photos above you can see a somewhat damaged red "anal horn". It is relatively delicate and will become limp and deflated if is gets damaged. E. labruscase has a similar anal horn during these early instars that it waves at predators when it feels threatened. We suspect the red anal horn of E. phorbas, would typically look similar and can be similarly "waved" when not damaged. This red anal horn will be lost by the final instar in both species, and replaced by a hardened black "button".

Final Instar:

When the caterpillar is threatened it adopts a posture where the anterior body segments are pulled in, while it inflates the thoracic body segments. The caterpillar appears to have the head of a snake, which probably helps protect it from attacks by its predators. What do you think, would this guy scare you?

Eumorpha phorbas caterpillar, final instar. Snake-like defensive posture - dorsal view.
Photographed by Kennedy Warne in Panama, see his original post here.

Eumorpha phorbas caterpillar, final instar. Snake-like defensive posture - lateral view.
Photographed by Kennedy Warne in Panama, see his original post here.

Close up of the anterior end of a final instar Eumorpha phorbas caterpillar in its posture - dorsal view.
Photo from Janzen and Hallwachs' database. Caterpillar from Costa Rica.

Remember that what may look like a "head" in the above photos are really just inflated body segments (specifically the thoracic body segments). The caterpillar's true head is actually relatively small in comparison, but can be seen if you look closely at the very tip of the "head" above. Inflating the thoracic body segments into a snake-like "head" isn't the only trick that this caterpillar has for scaring off predators. Where the caterpillar had a bright red anal horn in the early instars it now has a hardened black "button" that the caterpillar can manipulate such that it looks like a blinking eye - but it's not a real eye. The only other species known to have a "blinking" eyespot like this is its close relative Eumorpha labruscae. 

Posterior end of a final instar Eumorpha phorbas caterpillar showing the hardened button capable of "blinking".
Photo from Janzen and Hallwachs' database. Caterpillar from Costa Rica.

Eumorpha phorbas caterpillar, final instar, showing the hardened button capable of "blinking"
Photographed by Kennedy Warne in Panama, see his original post here.

I have written about this "blinking" eyespot in a previous post here. A more complete description of the "blinking" eyespot in the two species and its possible function in deterring predators can be found in our recent manuscript published in the Journal of Natural History:

Hossie, T.J., Sherratt, T.N., Janzen, D.H., Hallwachs, W. (2013) An eyespot that “blinks”: an open and shut case of eye mimicry in Eumorpha caterpillars (Lepidoptera: Sphingidae). Journal of Natural History DOI:10.1080/00222933.2013.791935

Still frames of a final instar Eumorpha phrobas caterpillar from Costa Rica revealing the hardened button, thereby creating what appears to be a blinking eye, at least to human observers

It may have struck you that the colour of the caterpillar in this final instar does not match the leaves of its host plant. From what we can gather it seems that the final instar larvae spend much of their time resting on the trunks of trees where it blends in among the lichen and moss, rather than sitting on leaves as it does in earlier instars. My correspondence with photographer and naturalist Kennedy Warne who observed a final instar E. phorbas caterpillar in Panama provides some anecdotal evidence to confirm this:

"Our specific interest was Pelliciera mangrove forest, but the encounter with the caterpillar was in in lowland forest abutting the mangrove area. The caterpillar was head-down, stationary and completely exposed to view, vertically oriented on a tree trunk covered with a fuzz of moss and liverwort."

Many of the species  from this genus burrow underground pupate below the leaf litter so this colour pattern may also help it blend in while it searches for a safe place amongst the forest floor. In our e-mail exchange Kennedy Warne also provided the following observations on the caterpillar's behaviour:

"We were struck by the fact that whenever we came close (perhaps six inches) from the critter, it slowly raised its head to assume a more snakelike pose. This was a slow movement, unlikely to have in itself caused a startle reaction in a predator (my conjecture) -- however the effect was to make the caterpillar more imposing, and certainly to reveal the full snakelike mien of the head. The blinking of the "rump" eye appeared to be continuous, perhaps every few seconds, though I didn't time it and can't remember the precise frequency. We searched nearby trees but this was the only specimen we encountered..."

These observations are certainly in line with what we had noted during our encounter with E. phorbas in Costa Rica. In a recent interview on a New Zealand radio show Kennedy Warne discusses his encounter. You can find the interview here; discussion about the caterpillar begins at 08:30.

Adult:

In the adult life stage this moth is relatively drab except for the small flashes of orange and black on the hindwings. The brown colouration probably helps the moth remain concealed on tree trunks during the daytime. A website run by Bill Oehlke reports that adults range in size from 112-121 mm wingspan and nectar at various flowers. They apparently breed continuously with adults reportedly caught every month of the year in Central and South America. In other related species the male moths track females at night by following pheromone plumes, and this is likely the case for this species as well.

Eumorpha phorbas adult (male), wingspan 112 mm. Arrows point to features for species diagnosis.
Photo from Janzen and Hallwachs database.

Eumorpha phorbas adult (female), wingspan 116 mm.
Photo from Janzen and Hallwachs database.

According to a note in the specimen record from the Janzen and Hallwachs database the colouration of the forewings can range from a more intense green to almost blue-black. Below is a different adult specimen with a slightly different colour as an example.

Eumorpha phorbas adult, wingspan 113 mm. Costa Rica.
Photo from Janzen and Hallwachs database.

More information about the adult lifestage of Eumorpha phorbas can be found at these links:

• Bill Oehlke's website - More adult photos and distribution information
• Lepidoptera Barcode of Life - Eumorpha phorbas
• Neotropical Moths - Eumorpha phorbas - Distribution and information on adult moths
• Encyclopedia of Life - Eumorpha phorbas - Photos of a caterpillar with slightly different colours

Find out more about "blinking" eyespots, check out these posts!

An eyespot that blinks?

Eumorpha labruscae: another caterpillar with a blinking eyespot