Mimicry, Shmimicry. It's the Fear, Stupid

Mimicry, Schmimicry. It's the Fear, Stupid.

What’s the reason for  the copy, or, perhaps as Yeats said, how do we know the dancer from the dance?

Two posts ago, I discussed mimicry in caterpillars and adult Lepidoptera again, mainly focusing on adaptations that allow these yummy bugs to hide in plain sight from all the creatures that want to eat them.  But this is really only half of the story. The other half – using mimicry as a kind of offensive weapon – is really more to the point when considering the case of the 5^th instar hickory horned devils and the spider mimicry that I have proposed their horns are helping them accomplish.

If camouflage is one way caterpillars and moths keep safe from birds and other predators, another is to develop a visual association with things these animals actively avoid – things that they find aggressive, unpleasant, or are outright life-threatening. If done effectively,  this is an even better strategy, because when the predator succeeds in discovering the bug, it still works. Birds and other predators actively avoid things that they are scared of. I say “if done effectively,” because mimicking a threat animal may, in fact, be harder to evolve working adaptations for than developing camouflage. Nonetheless, there are a lot of examples of effective fear-based  mimicry in nature, so it can’t be that hard.

A common kind of offensive mimicry in caterpillars is to evolve color spots that look like eyes, so as (obviously, due to their long, cylindrical shape) to look a bit like snakes.  Birds really do not like snakes, for good reason – snakes are one of their few predators that can get up in the trees. Here are a few examples of caterpillar-snake mimicry:

Eye spots are apparently relatively simple to evolve through changes in the genes that affect surface coloration, which may contribute to this being a popular (commonly arrived at through the forces of natural selection, that is) survival trick.  Eye spots also occur a lot in adult moths and butterflies, especially in larger ones – for instance among the giant silk moths. Here are two different North American examples:

Io Moth

Polyphemus Moth

Obviously moth eye spots are not there to mimic snakes, so what is the function? Well, birds have other predators as well in the trees – climbing mammals such as raccoons and opossums (and squirrels, which, believe it or not, sometimes eat bird), and especially hawks and owls. Behavioral biologists generally assume that the wing spots on moths are there because when a disturbed moth flashes them it gives an attacking bird the shock of thinking that it has stumbled on an owl.  If you are a small bird, always on the lookout for ambush attacks from these winged predators, this would be a very nasty surprise and an effective scare.

“Avoidance,” which we humans think of as a rational, learned thing, is actually more a behavioral adaptation in nature, and an unseen property in ecosystems. Creatures living in the natural environment have a day-to-day struggle to stay alive: to not be eaten, to not starve, or to not fall into a state (through lack of food, injury, sickness, etc.) where they cannot maintain the strenuous activities they absolutely must perform daily to keep living. Generally, they have no backup, no support system, the way humans do with our human society. Consequently, when there’s something that is pretty constantly bad/dangerous/risky for them in their natural environment, natural selection tends to evolve an automatic behavior in the animal’s population that causes them to avoid the risk – natural avoidance . Let’s call it an instinctive fear.  Humans can’t see these instinctive fears in nature directly (you’d have to be inside the bird’s head), but it can be a real thing, with really obvious signs – a pattern in the ecosystem, if you like – that you can detect indirectly.

Take the strange pattern of the commonness of blue-black butterflies in the American South.  Here are a few examples – notice the common pattern:

How do we explain the commonness of this pattern of colors? Okay, you might say, these are all swallowtail butterflies – they are all related to each other, so maybe they’ve all just inherited the pattern from a common ancestor. But then consider these two butterflies, which actually come in two different color forms,  a blue-black form, and one that is not:

Red spotted purple (Limenitis arthemis)

Banded purple (Limenitis arthemis)

Eastern Tiger Swallowtail (dark form)

Eastern Tiger Swallowtail

Notice first, that the red spotted purple is not related to the swallowtails (it belongs to the brush-footed butterflies, a very different group) and that the different forms of the two species are really different in appearance. One form of each is blue-black, while the other has vertical stripes. (Vertical stripes are an interesting defensive adaptation that helps flying butterflies survive bird attacks by making it difficult for the bird to distinguish between the butterfly’s body and wing when it is in motion – if the bird pecks the wing, the butterfly gets away.)

A key piece of information to note is that the blue-black forms of these two butterflies are not common everywhere in each butterfly’s range: they are only common in the south. When I collected butterflies as a kid in Ithaca, NY,  I never saw a red spotted purple or a dark form tiger swallowtail though banded purples and regular tiger swallowtails were very common.  But when my family traveled about 100 miles south (say, to Long Island or Pennsylvania ) I did finally see these elusive insects and collected them excitedly. I was really confused why they were so common a relatively short drive away.

There is a reason – the pipevine swallowtail (the first photo in the series) feeds pretty exclusively on the toxic southern plant pipevine and, with that plant, has a range whose northern limits are about at Long Island and central Pennsylvania. The poison the butterfly gets from its food plant is, apparently, very toxic to birds – so toxic, in fact,  that birds are really afraid of it (avoidance again), and other butterflies (none of which are poisonous themselves) have adapted (though natural selection) to take advantage of this fear through mimicry of the pipevine swallowtail.  This is a kind of mimicry that biologists call “Batesian Mimicry.”

I’ve read descriptions of how this works that go basically this way: “any bird that tastes a pipevine swallowtail has such an unpleasant experience that it doesn’t ever forget it and any butterfly that looks like the noxious one gets left alone as well.”  Is this what is happening?

As a human, it’s natural to imagine it this way, since we learn most of the avoidance we practice – like learning that the flame on the stove is hot, etc.  For birds to learn the poisonousness of butterflies this way however, seems somewhat unlikely – it would likely take a little while for the association of sickness with the specific insect to be learned, and birds only live a year or two. It seems likely that only a small part of the bird population would be experienced enough to practice avoidance. There’s also the issue of how clear a lesson birds are being taught, given all these harmless, tasty mimics that are perfectly good to eat also flitting around the birds. In my observations, both here and in other parts of the south, pipevine swallowtails are not rare, but they are by no means the most common of all these insects. If you were a bird regularly eating blue-black butterflies, and only occasionally ate one that made you sick, how long would it take for you to get the message? A while, I think. If each bird has to learn for itself not to eat a blue-black butterfly, the result seems hardly likely to be effective enough to make mimicry an effective adaptation – which it must be.

So let me propose a slightly different hypothesis that I think makes a little more sense, given all the evidence of mimicry: I propose that the toxin that is in the pipevine swallowtail can be seriously dangerous to birds’ health, having a significant impact on their ability to survive.  If the toxin is this harmful, natural selection would favor the development of an instinctive fear (natural avoidance again) of butterflies that look like that. This instinctive fear is really a simple, built-in behavioral rule that keeps the birds away from that particular form of harm (like a built-in fear of snakes and owls, or like my fear of spiders).  This behavioral rule is powerful and widespread (it evolves in many species for the same reason), so natural selection (in turn) favors many other butterfly species adapting to take advantage of its invisible presence. It doesn’t matter that most of them are perfectly good to eat – natural selection has hardwired in a dislike for black butterflies as a general principle, so if they evolve black coloration the avoid being eaten.

Pipevine -- a pretty plant, but the source of birds fearing
black butterflies.

My basic point here is that there are features in the landscape you can see directly (watch an owl eat a songbird), but there are also important forces out there that exist invisibly (in behavioral adaptations, like fear of black butterflies for example) that you can’t see directly. You can, however, still come to understand what these forces are by looking for patterns (common forms of mimicry, in this case) that provide clues.  In some ways,  I think it can be more exciting in nature study to see the invisible than it is the visible.  Who would have known that the innocent little pipevine plant could be responsible for  a significant piece of predator-prey behavior in eastern North America or for making many butterflies in the south black? Perhaps something similar is responsible for the bright coloration of the adult regal moth, but I’ll leave that for a later post.

Conjuring Nature’s Ghosts

Conjuring Nature’s Ghosts

In my last post, I pondered what survival strategies  the hickory horned devil caterpillar could be using in the middle stages of its larval life. On the one hand, they are not huge and threatening yet, and clearly not toxic to predators (no toxic foodplant, no stinging spines). They also are an inconvenient color (brown) among the green leaves they feed on during the day. This should be a recipe for disaster…

But they do have these freaky looking horns – harmless spines that are kind of like antlers. These can’t be easy to handle when you’re a caterpillar crawling around a tree… which means there must be some advantage to having them.

Looking at them a bit more, I remembered something from my own past experience. I actually had seen a hickory horned devil just once before raising them. Seven years ago, I was new to Charlotte, and out walking my dog in my neighborhood.  Watching the dog sniff things, I noticed some large caterpillar droppings on the pavement. I looked up, and there, just above my head, was a fifth instar hickory horned devil clinging to some sweet gum leaves. I jumped back, which, for me, was an odd reaction to spotting a spectacular caterpillar. As you’ve probably figured out from reading this blog, I think caterpillars are cool and I’m not at all frightened of them.

But I am, inexplicably, frightened of spiders (I always have been) and there was something spiderlike about this caterpillar. My spider fear is literally instinctual (I say it’s “hard-wired”) – I generally have no fear of other bugs, even ones that bite. This is actually a common human fear (psychologists call it “arachnophobia”) and I’ve read scientists who theorize that many of us come with it built into our brains because, in the distant past, our ancestors lived in places where spiders were frequently dangerous, so evolution has favored a built-in fear. I believe this, because it is definitely something primal in my brain, like a fear of barking dogs or of snakes.

So, look again at the photo of the fourth instar caterpillar above and look at these orb-weaving spider photos:

Notice the similarities between the spiders’ conspicuous legs and the caterpillar’s spines? There are eight large spines, and even in the fourth instar, they look distinctively like these native, long-legged spiders. Yuck.

And I can tell you (with an inner quiver) that we have a lot of these spiders in Charlotte, hanging their webs from tree branches. In August, about the time the hickory horned devil caterpillars reach their fourth and fifth instars, orb weavers also mature and come down out of the treetops where they have been growing in obscurity and hang their webs out in the open. At this time the hickory horned devils are becoming so large that they too become conspicuous.

Why would a caterpillar mimic a spider? Spiders bite, but these spiders are not dangerously venomous like, say, the black widow spider… one wouldn’t expect birds to be afraid of them because of that. Of course, they are dangerous to other insects, particularly to flying insects…

So here may be our answer – you may remember that I mentioned in earlier posts that parasitic wasps are one of the biggest dangers that giant silk moth caterpillars face, destroying large percentages of every brood. A big spider is a dangerous predator to a little wasp. The hickory horned devil’s spider mimicry may frighten away the parasites.

But, thinking about it, there still may be an effect here on bird predators as well. I’ve always found it puzzling that big orb weaving spiders (like those whose photos you see above) are so conspicuous – large, brightly colored, hanging in the middle of the web with no cover, where a flying bird could easily pluck them.  Yet birds don’t. I did a search of the literature on bird predation on orb weavers and found that biologists find that bird predation appears to be uncommon. In nature, bright coloration is sometimes a sign that an insect is toxic and not good to eat. Yet again, there is no mention of this in the literature – surely someone has looked into these big arachnids  being bad tasting… They are not poisonous in bite or taste, yet they advertise their presence… hmmm.

So let me propose an alternative –perhaps birds leave orb weavers alone because they are hard-wired to be instinctively frightened of large spiders just like I am, though there is no longer a real threat in these particular bugs.  In the tropics there are large orb weavers that are more venomous and sometimes prey on small birds. In other words, evolutionary history has given large spiders a fearsome reputation, and, though they may not still deserve the fear, they are still using it for protection. And so does the hickory horned devil… Deep instinctive fear is a force and it has echoes.

See -- totally harmless!

History has meaning to humans because we learn lessons from it.  In the battle for survival that we call nature, some lessons have value for other species as well, and they too find ways to preserve the history.

Anyway, it’s a hypothesis.

Who Cares How You Look?

The birds do, Mr. Doo-doo.

After my last post, I have to say that the hickory horned devils are now second instar and, ahem,  big enough to be outside now, and everyone is happy about this, especially the hickory horned devils.

(I’ll talk about the arcane practice of “sleeving” caterpillars in a subsequent post.)

Each time a caterpillar sheds its skin to grow larger, it is said to have entered the next “instar.” The hickory horned devils are now in the second instar out of five. Some caterpillars look pretty similar in every instar (lunas, for example), but some change their appearances fairly significantly. Hickory horned devils are in the latter group. They are about an inch long and look like this:

What do you notice about the appearance of second instar hickory horned devils? Well, to birds they look like bird poo… or so entomologists think (who really knows what birds think?).

A fairly typical bird dropping. Yes this is gross – but the demands, of science, etc. If you look carefully at tree leaves, you see this all the time because a lot of birds perch in trees.

 Why do they see that in this harmless little caterpillar? Well, the splotchy pattern and the squiggly curve of the body does look a bit like the dropping photo, but this is also something that they have seen before in the bug world. Here are some other examples from both moth and butterfly caterpillars:

Viceroy butterfly caterpillar

 "Orange Dog" -- caterpillar of the giant swallowtail butterfly

Moonseed moth caterpillar

Ruddy daggerwing butterfly caterpillar

Sure, these caterpillars look pretty different from each other (and from the hickory horned devil), but you see the overall pattern – bumpy shape, white splotches mixed almost randomly with other colors, especially dark browns. Behaviorally, each of these caterpillars tends to rest curled in a questionmark shape. You can see the resemblance with the bird poo and with the hickory horned devils (though my photos aren't great).

Why do so many caterpillars use this kind of camouflage? (This is actually a form of what we call “mimicry” – but much more about that in later posts.) Well, there are some obvious answers. First, it’s a common pattern on tree leaves, so it really is a good pattern to copy if you want to blend in. Second, to birds it looks like… poop. Most creatures have a built-in dislike for putting that stuff in their mouths (or even getting near it) because being in contact with it is a great way to catch diseases from your fellow creatures. Think about your own disgust – it’s hardwired in us by evolution.  Though not all species share this built-in disgust  or “aversion” (dogs come to mind as an counter-example) to feces from their own kind, it’s common enough to assume it’s likely to be present in many birds.  

So that’s why this appearance pattern works as a survival “strategy,” but how did so many different kinds of caterpillars come up with it? (I’ve only shown a few examples – there are hundreds, if not thousands  of others out there.) You need to remember here that bugs don’t actually consciously “come up with” these natural tricks that help them survive, any more than you “came up with” your natural hair or eye color to make you look cool and attractive to other people.  The caterpillars’ appearance was, originally, the result of a random set of mutations -- or a random new combination of existing genes -- that accidntally happened to create this appearance. But the pattern happened to work for the bug that first was gifted with it by chance, and it survived ... and made a lot of similar bugs that also survived, and so the genes – the genetic instructions for how to look like bird poo – got passed on and became common. Because the trick works, the genes then stay common, even as the species evolved and passed on its genes to many other species, its ancestors.  This is basically how natural selection works on genes over time – genes that have a lot of usefulness stay in species’ genomes because they keep coming in handy in staying alive.

From the examples I showed above, you might have caught the fact that there are both butterflies and moths that use this pattern.  Think about what this means – biologists know pretty much for certain that all butterflies and moths are relatives – they have evolved from common ancestors, with butterflies first evolving from moths about  100 million years ago (this is a guess, of course – the oldest fossils of butterflies are about 48 million years old, but these fossils are very modern butterfly-like, indicating that the split from moths had to be earlier).  This means that genes that are shared between moth and butterfly species would have to be pretty ancient – at least 100 million years old.  I would guess that the basic genetic package for the bird poop-camouflage trick has to go way back  and still be hidden out there in the genes of most butterflies and moths for it to currently be so common in this group of animals.

Of course there is another possible explanation – it’s called “convergent evolution” – where different species independently “come up with” the same common set of features because, well, it works. This is possible here. The thing is though, for so many different varieties of moth and butterfly to come up with this same pattern there would still have to be some common underlying feature (a broken white/color pattern for example) in order for it to come up again and again and again. A better bet is that the bird poop imitation was so successful for the moth/butterfly ancestors that it stayed around long enough to eventually drift together on the genome as a kind of package -- a big and complex group of genes that is a fundamental tool for survival through the bird poop trick.

What’s fascinating to me about this kind of thing in caterpillars is that you can literally see the animal taking advantage of different parts of its genetic heritage as it grows up and its situation changes. When the caterpillar is really little (and too small to be mistaken for bird poop), it doesn’t look like this at all, as we have seen.  When it gets bigger, it’s too big to be mistaken for bird poop, and so its appearance changes again. But when the caterpillar is in its second instar, it is really just about the right size, so the time is right for natural selection to again pull these genes out of an ancient bag of tricks. Pretty cool, I think, the way you can see all kinds of pieces of ancient history coming out and showing itself to you in a living bug.

Bibliography

Wagner, David L. 2005. Caterpillars of Eastern North America. Princeton University Press, Princeton.

Scott, James A. 1986. The Butterflies of North America. Stanford University Press, Stanford.

Imagining the Moth

The female regal moth I caught on July 26 was dead by last night, having laid 135 eggs (which entomologists call “ova” – scientists like to have their own jargon) . I’ve cut them out of the cardboard container I kept her in and put them in the clean glass container you see above for careful monitoring. The standard egg laying container is a paper grocery bag, but I didn’t have one, so I made due with  a stationary box, which did the job. They are the largest lepidoptera (butterfly/moth) eggs I’ve ever seen and they are a beautiful translucent green, except for a few, which are now partially brown. Those are that way because the eggs are transparent and you can actually see the embryonic caterpillars developing inside – the brown is their heads—I’m guessing some will hatch tomorrow. I have saplings of their foodplants ready in pots – when they are really little I want to grow them inside the house where I can control the environment.

Before you feel too sad for the moth who died for this , I need to say don’t fret – she accomplished her primary mission in life: laying eggs. Giant silk moths only survive a few days as adults in the wild, living entirely off fats that they accumulated as caterpillars. They have no functioning mouthparts and they don’t eat.  They have only two missions – to mate, and to lay as many eggs as possible.

I”ll talk about their mating behavior another time (because it’s an important topic), but their egg laying is also interesting. Regal moths, like many of their close kin, often fly great distances, depositing an egg or two on one tree, then flying a quarter mile to lay another egg. There are a lot of possible explanations for how this behavior evolved.(I like to call these “explanations” “hypotheses” because no one actually knows how the pressures of nature encouraged the behavior’s development, and, frankly, it’s hard to imagine an experiment that would prove the “real” cause. Honestly, what follows is all unproven speculation – intelligent guesses. In science, the next job would be to find some clever way to test these ideas – to design an experiment and then collect solid information – “data..” However, nature – the world outside is a messy, complicated place and coming up with intelligent designs for such experiments is very, very difficult. For now, I’ll stick to the fun, imaginative part – the hypotheses.

 My personal best guess  for why regal moths have evolved to fly long distances and lay single eggs is that, since these eggs grow into very big caterpillars, it would be a bad idea for too many of them to be on one tree because they are likely to attract the attention of predators (such as birds) and once a predator has found one caterpillar, it is going to be primed to see another one nearby. So, this hypothesis says I saved the female moth the effort of flying all over the forest to lay her eggs, so she probably was able to get more laid before her fat-stored energy ran out (fat is really just a chemical battery, if you think about it). She had to lay them all together, which might be disastrous in nature where there are birds, but I’ve got her back – I’ll protect her caterpillars from predators. This makes me the good guy. Really.

However there is another “hypothesis” for why this moth has evolved single egg rather than mass laying behavior and this explanation perhaps means that I’m not being so clever in “farming” these caterpillars. Some of the regal moth’s near relatives, the oakworm moths (species in the genus Anisota), do tend to lay their eggs in big masses, and the caterpillars feed together in big troops, especially when they are young. (Herding together must serve some kind of protective function for these caterpillars, like it does for bison and schooling fish and ducks and starlings and the like, but I have no idea how that works – make your own hypothesis.) Oak moth caterpillars are considerably smaller than regal moth caterpillars at maturity and they grow up faster. Importantly, this means they have less time chance to catch a disease that could spread from caterpillar to caterpillar quickly, wiping out all a moth’s brood in one rapid epidemic.

       Young oakworm moth (A. osalari) caterpillars. National Park Service photo by Sally King.

This is a familiar problem to anyone who has ever tried to raise a lot of giant silk moth caterpillars  – you have to grow them in crowded conditions (you’re really “farming” them) and various diseases can appear and destroy your project. So perhaps another explanation (hypothesis) for why the regal moth lays single eggs is that this protects long-maturing caterpillars from spreading the diseases a few are likely to catch during a long period of infancy. This could be the explanation, or both explanations could be right or… something else entirely might be the cause. Nature is complicated and it’s hard to imagine all the problems that might come up in the life of a moth.

But it’s still fun to make guesses about the evolution of unusual characteristics in a species. One other feature of regal moth egg laying behavior that I also think is a bit strange is the fact that these moths produce only one generation a year, even here in the south where summers are long. This is actually not typical of most giant silk moths. Lunas, for example, have at least two generations a summer here in North Carolina, and researchers have noticed that they have three in Texas. The first lunas hatch and lay eggs in April here, but the regal moth waits until the end of July or August to hatch, mate and start laying eggs. Why?

We can reject the explanation that the moth has only enough time for one generation a year because it is so big that it takes a long time to grow. It does take a relatively long time to grow, but not really that much longer than a luna, which goes through the whole cycle twice. So let’s add another piece of evidence: its closest relatives (other species in the sub-family Ceratocampinae) also have only one generation (one “brood” as scientists say, or “univoltine” behavior) though many are much smaller moths. The authors of The Wild Silk Moths of North America  have suggested what I think is a convincing hypothesis for this: “In the United States and Canada the greatest number of species occur in the Southeast. Midsummer flight in warm, humid weather maybe an adaptation related to the tropical affinities of the group.” In other words, the authors note that relatives of these insects are a lot more common in the American tropics, so species like the regal moth may represent relatively recent invaders from tropical climates and they may still have hold-over physical adaptations from their not-too distant past, such as favoring the time of the year when North Carolina feels like Mexico or Honduras. In the tropics, the moths lay eggs in the rainy season, since that’s when the food plants are freshest. Perhaps these tropical moths have carried the home country behaviors here.

 This is another perhaps un-provable hypothesis regarding evolution, but I like it because it again makes you expand your imagination to consider yet another dimension that can affect things: history. Consider the fact that only a little over ten thousand years ago (a blink of an eye in biological history, really) most of North America was covered by the expansion of a thick ice sheet. (Ice might have been a mile thick where I live now.) When that happened, where did all trees, bugs and other animals go? They either died out or they moved south to where there was no ice (Florida would have been ice free, but much cooler than now.) Then, when the ice receded back to the north, old species returned and some new species invaded from the south. The regal moth and its relatives may have been just such invaders – they still carry the signs of their history in the way they live.

So, in order to come to grips with how a moth works you need to imagine all kinds of things – what it’s really like out there – and what it must have been like out there a long time ago. Who knows what the most important “causes” were? There were certainly many, all working together and the result of the biological evolution they caused is the moth we have now. To really know we await clever minds, brilliant experiments and … data.