Regular Diane G., whom I thought was mostly into birds, sent a bunch of Monarch butterfly pictures as well as an extra lep species. She also has two questions for butterfly mavens—see after picture #4:
Last Friday I was birding on the shores of Lake Erie, at a site that consisted of several large impoundments bordered by causeways, when I noticed a flutter of Monarch Butterflies (Danaus plexippus) at my feet. They apparently were drawn to a rather unattractive plant managing to eke out a living in the dry graveled surface of the causeways.
I reflexively pointed my camera down and grabbed just a few quick shots, being primarily interested in birds. Later I became more intrigued when I had a look at my pictures and noticed that the butterflies were extending their proboscises (proboscides for Diana), not to the minute, difficult-to-notice flowers of this nondescript herb, but instead apparently to the surface of the twisty gray, hairy leaves themselves. (I suppose it’s possible they were merely searching for the flowers, but somehow one expects butterflies to be more adept than that.)See tiny flowers here, to the right:
And proboscis here:
And I’ll throw in one of the few spread-winged shots I got, though my shutter wasn’t fast enough to stop the wing closing action that began as soon as a butterfly touched down:
So–I’m wondering if any of our resident entomology experts can explain this behavior? (The name of the plant would be appreciated as well.)And speaking of lepidopterans, I snapped a few shots of this lovely Common Buckeye (Junonia coenia) the same day:
(Excuse the lack of paragraph spacing below; I can’t seem to fix it.)
By the way, our resident butterfly evolutionist, Dr. Marcus Kronforst, informed me that the Monarch/Viceroy “Batesian mimicry” story is bunk—or at least more complicated than conventional wisdom dictates. People have been saying this for a while, but I wanted to ask an expert. Let me recount the story.
The classic tale is that the Monarch is unpalatable because it eats mostly milkweed, which renders it toxic and sickening to bird predators. (Milkweed contains cardiac glycosides, which the butterflies sequester in their bodies, probably as a defense against predators. A Monarch fed on non-toxic plants is perfectly edible). The bright black-and-orange of the monarch was supposed to be “aposematic”: a warning coloration that says “don’t eat me” to birds. (I won’t get into the evolution of aposematic coloration, as it’s complicated.)
The Viceroy butterfly (Limenitis archippus), also North American, was supposed to be tasty and edible, but gained protection from bird predation by evolving a mimicry of the Monarch’s colors and pattern: a resemblance called “Batesian mimicry” after the British naturalist H. W. Bates. Birds entrained on the Monarch pattern would simply avoid taking Viceroys. I taught this as the classic example of Batesian mimicry for years, and it was in all the textbooks. (I am sure creationists will hop on this, for they haven’t learned that science advances, and truths are provisional.)
The mimicry between these two largely unrelated species is striking, but the story isn’t quite correct. Here’s a picture from A Network of Ideas, which presents the erroneous story and also gives an incorrect characterization of the butterflies’ palatability.
In fact, in many places the “palatable” Viceroy is actually unpalatable, eating toxic compounds that also render it distasteful to predators. In such places the mimicry may be of a different form: Müllerian mimicry (after the German naturalist Fritz Müller), in which two unpalatable species mimic each other. Natural selection would favor a convergence of color and pattern among unpalatable species, for by resembling something the predator has already learned to avoid, you would minimize your chances of being attacked and killed—even if the predator does spit you out after it tastes you. So in places where both species are distasteful, we have a case of Müllerian rather than Batesian mimicry.
But in other places Viceroys are tasty and nontoxic as they don’t eat plants whose compounds make them distasteful. In those places the mimicry might truly be described as Batesian.
That still leaves the question of how the system began. For surely the resemblance to Monarchs did not evolve twice in Viceroys independently, in some areas as a Batesian pattern and in others as a Müllerian one. But once the resemblance did evolve, it could be useful no matter whether the Viceroy was toxic or not. Which evolutionary process came first? Who knows?
Finally, as I’ve implied, things can get quite complicated. In some parts of the world a single pattern can serve to enforce both Batesian and Müllerian mimicry. Here’s a figure from Wolfgang Wickler’s classic book Mimicry in Plants and Animals (1968) showing three instances of what are called “mimicry rings.” Each column represents a series of diverse species from one area that resemble each other. Those species above the gray bar are said to be Müllerian mimics of each other: they are all distasteful. Those similar species below the gray bar are said to be Batesian mimics of those above: they are all tasty and evolved a similar pattern to species above the bar as it would reduce predation. Remember, each butterfly is a separate species. The resemblance among species within each of the three groups is remarkable.
Now, you might ask yourself, how do we know which species are distasteful and which are edible? I don’t know the answer, but I suspect that biologists simply tasted them! Hairy-chested field biologists (males, that is) often will pop insects into their mouths, assuming that if it’s noxious to them, it’s noxious to predators. Dan Janzen, a famous naturalist who was the head of my Tropical Studies course in Costa Rica in 1978, used to do this. I’m not sure, though, whether that’s a good test!
The best way would be to use the same method Lincoln Brower did when he demonstrated that Monarchs are toxic. Give a Monarch to a naive, hand-raised bird (he used blue jays). The naive jay noms it eagerly. A few minutes later, the jay gets queasy and vomits. When presented with another Monarch, the jay freaks out and won’t eat it. Only one experience is sufficient to teach the bird to avoid the pattern. This shows that the Monarchs are toxic and that birds can learn quickly.
Here’s the classic series of photos of a naive jay nomming a Monarch and then throwing up shortly thereafter:
Brower also showed that an entrained bird avoids Viceroys as well, although they’ll nom them eagerly and want more if they haven’t previously tasted a Monarch. This is the experiment that led to the notion that Viceroys are tasty and are avoided because they resemble monarchs, which birds have tasted and rejected. And that was the classic demonstration of Batesian mimicry.
Now I’m not sure if Brower used Viceroys taken from an area where they are indeed palatable, but, as I said, the story is more complicated than this. Had he used the toxic races of Viceroys, he might have concluded that they are Müllerian rather than Batesian mimics. In fact, regardless of how the system evolved, Viceroys are Batesian mimics of Monarchs in some places and Müllerian mimics in others.
Those are good Monarch pictures. I’ve been trying to get some pictures of them out my front door, but I need a new camera. I always wondered if birds ate them…hopefully one time is enough to make then never do it again.
Or maybe you need some lessons in technique? Good technique can get good images out of a pretty poor camera when an incredible camera can still take photos of your boot tips and lens cap.
(Earlier today, I was putting a note in my diary for a session on wildlife photography being run by the local “Science festival” type thing. I hope I’ll be on the correct continent to attend.)
No idea what the plant is, but suspect it’s one of those that end in wort.
Very cool, and nice Monarch photos. I really enjoyed the fuller story of the Monarch/Viceroy mimicry. Thanks!
I think I know what the monarchs are feeding on, but I will leave that to others.
I had first learned about the ‘truth’ of viceroy/monarch mimicry waaaay back in grad school, but I did not know it was a more nuanced case where the old idea that it was Batesian mimicry is also true in some/many cases. I suppose which sort of mimicry evolved 1st would depend on which one was more common.
butterfly 😀 like it 🙂
To test butterfly palatability, my entomologist friends at the University of Texas in the 1980s would capture tropical birds temporarily and feed them different kinds of butterflies to see how they reacted.
Uh, huh. I hear Sithrak oiling a special spit. No particular reason. Just a spit. For roasting. Something bigger than a chicken.
Mmmmm…I love roasted turkey!
b&
I’d like to try swan, it must be pretty good because it was saved for royalty in England, but nowadays they’re all protected I think.
Lovely photos.
I remember going up to the Adirondacks each summer, and seeing monarchs among the milkweeds. I remember going to the beach in September and watching what seemed like droves of monarchs flying along the sand.
I haven’t seen a single monarch this year. I don’t think I saw one last year either. It’s depressing.
We saw quite a few on our hike in Ontario a couple of days ago. Loving the goldenrods.
The plant looks like a forget-me-not (Myosotis laxa), but I could be wrong.
Were there any hemipterans on the plant? Things like aphids, scale insects, etc., that might be producing honeydew? If so, the leps could be feeding on the excess honeydew that is produced by them. I couldn’t see any obvious aphids or their ilk in those picture but they tend to be small anyway.
I see sooty deposits (‘honeydew’ is the feces of aphids), so you are probably right.
Forget-me-nots don’t have silver-green fuzzy foliage at least not the ones in our garden so I am ruling those out. So far, I am unable to identify this plant.
Honeydew may emerge from aphids’ anuses, but it’s not feces.
http://en.m.wikipedia.org/wiki/Honeydew_(secretion)
I had thought some of the specks on the plant resembled mealybug-type scale insects, and hypothesized the honeydew aspect myself. Was interested to see if anyone else brought it up. 🙂
Once the mineral/salt possibility was mentioned below, though, that became my favorite hypothesis; especially since none of the specks really look too scale-like when zoomed in (it’s hard to be sure, though).
Are there any non-toxic Monarchs? If so, that could further complicate the evolutionary web…especially if their range overlapped with toxic Viceroys….
b&
Some milkweeds have very low concentrations of cardenolide which make the monarchs toxic. I’m not sure if they are entirely unprotected though.
As a side, this protection extends not only to predators but also to parasites. See here for a paper about how these compounds also protect against infection (probably behind paywall, I’m checking from work): http://onlinelibrary.wiley.com/doi/10.1111/j.1461-0248.2010.01537.x/full
Thanks. You’re right about the paywall.
You also remind me of one of the more environmentally-devastating aspect of RoundupReady crops…the overspray from liberal application of Roundup is killing what little milkweed remains, and that’s taking out monarchs and other critters that rely on it….
I don’t oppose GMO crops because they have different genomes. I oppose them because the megacorps that produce them act irresponsibly like this, and because of the bullshit patent games they play with them, and because of the monocultures they create, and….
b&
Those are good reason to oppose GMO. Many do so on the basis that it will lead to horrible mutants that escape captivity and terrorize, and destroy everything in their path, and…
The Day of the Triffids, mostly.
I agree with your views. So many of the anti-GMO crowd make unproven claims about GM plants. But the definite problems include the factors that you describe.
Those problems are not the fault of GMOs. They’re the fault of corporate monopolies on GMOs. The solution is not to oppose GMOs, but to break the monopolies by creating a diversity of public domain “open source” GMO crops.
No, most of the real ecological dangers are due to the GMOs themselves, and would be present no matter how they were marketed or by whom. Some GMOs escaping into the wild (for example, those with bt toxin genes, or possible future GMOs with frost resistance) are at least equivalent to introducing highly invasive non-native plants. I suspect they could have a much bigger effect on ecosystems than some of the worst non-GMO plant introductions (which have devastated huge areas in the US, though non-botanists hardly notice). Imagine the selective advantage a weed would have if no insects could eat it, because it contained genes for production of bt toxin.
Having lived in the cornbelt for the past 45 years I know that there is no shortage of milkweed. Two things have happened. One is that the hedgerows (which seldom had “hedges” in this country) have been carved narrower and narrower until, as I used to teach, they were reduced to “one weed wide.” This does eliminate a lot of habitat for both plants and animals and provides the farmer with a few bucks more corn money (combines can cost more than half a million dollars). The real problem comes from the Mexican end of the monarch story where despite laws protecting monarch wintering groves these laws are pretty well ignored and the locals have cut down almost all the wintering habitat for charcoal. This is what is really destroying monarch populations.
Yes, it’s not about oppose GMOs as such, but opposing the corporations who make them.
I believe it’s a type of saltbush (Atriplex). If you look at the wikipedia page, it says “Atriplex species are used as food plants by the larvae of some Lepidoptera species.” I was going more in the direction of butterfly puddling behavior, which made me think of the salt levels in saltbush.
I’ve been raising monarchs all summer. What a fun hobby! No caterpillar deaths out of 14 – better than their chances in the wild. I’ve also encouraged neighbors to plant milkweed to help the monarch populations rebound.
I cannot find a picture of Atriplex with flowers like the one above. I suggested above that it looks like a forget-me-not, but there is a difference in the hairiness of the leaves, so I am not positive.
I certainly agree that the butterflies were feeding on them b/c the leaves were exuding salt. The buckeye butterflies on the ground were likely also looking for this resource on the soil. Flower nectar is low in mineral ions and other essential things, and butterflies often supplement by drinking from puddles, manure, and even dead carcasses.
There’s another reason butterflies visit plants, besides food or salts. Many tropical species actually acquire poisons from plants as adults. Plants of the family Boraginaceae, Asteraceae, and others are often involved. An example of a group of butterflies that do this is the Ithomiinae butterflies, which coincidentally are often part of mimicry complexes that include Monarch-like warning patterns.
Here’s an article abstract on one example of this:
http://www.nature.com/nature/journal/v309/n5970/abs/309707a0.ht
I wonder if you’ve discovered that Monarchs also do this???
Wow.
We could be witnessing the birth of a new scientific paradigm. Web-based discovery…WBD.
That sounds fascinating–I’d never heard of adult-acquired toxicity!
Alas, your link must be pay-walled–it takes me only to the front page of nature.com. Wikipedia has what seems to me like a nice write-up of this group, though:
http://en.wikipedia.org/wiki/Ithomiini
Especially interesting (to me) is the bit about the butterflies scraping wilted plant tissue with their legs in order to suck the sap; nectar I can understand, but I didn’t think butterflies were capable of much else!
(I doubt there’s much left of discover about Monarchs…?)
Yes, mineral “puddling” makes very good sense. Thanks for the reminder.
Back in the 70’s, a friend of mine, Karen Feeny was doing (IIRC) some of the first work regarding puddling; I remember thinking her method was so simple & brilliant–artificial puddles with various substances added, then pictures showing all the leps around the salt puddles…
“I was going more in the direction of butterfly puddling behavior, which made me think of the salt levels in saltbush.”
Ah, I finally have an explanation for something I didn’t understand before. I once saw a butterfly repeatedly engaging in what seemed to be pissing on my bare leg, and then licking it up. As a means of obtaining salt, it finally makes sense.
I was thinking Verbascum lychnitis
(es.wikipedia.org/wiki/Verbascum_lychnitis). The article isn’t in English, sorry, but you get the picture.
But now I’m thinking you could be right about Atriplex. The butterflies are probably taking on salts. I’ve seen blue butterflies (possibly blue morpho) taking on minerals from the patio slabs where the dog had urinated.
(en.wikipedia.org/wiki/Atriplex#mediaviewer/File:Atriplex_elegans.jpg )
Atriplex seems like a very good candidate–thanks, Bluestem!
The monarchs must be migrating. I had some larvae on my milkweeds this year and I’ve seen some monarchs around now so they are probably on the move.
That poor puking jay – yuck!
Thanks for the proper plural of proboscis, Diane. 🙂
🙂 The Greek seems much easier on the tongue!
I suppose this might be the start of migration time. The butterflies here also look to be in pristine condition, which suggests that they’ve only recently emerged.
Responding to Ben’s comment (10) above, it does seem like there is variation in the toxicity of Monarchs. Monarchs winter in large roosts (colonies?) here in Santa Cruz and several years ago one of my colleagues had a student study predation on the butterflies. I heard the story second hand (don’t think it is published) so the details are sketchy but if I recall correctly one or two of the local bird species (chickadees?) figured out the Janzen test for themselves and they tasted butterflies by nibbling on their wings. They spat some out and ate others, presumably the result of variation in toxicity and taste.
Clever little chickadees!
I’m far from expert, but my guess on the mimicry question is that Müllerian came first. Once the Viceroys were protected from predation by Müllerian mimicry, it then became safe for them to opportunistically switch their diet to nontoxic plants, which in turn allowed them expand their range to areas where Monarchs were present but the Viceroys’ normal toxic food source wasn’t.
But again, I’m just guessing.
Sounds reasonable to me.
An advantage to being able to switch to non-toxic plants is that there can be considerable energy cost in sequestering the toxins. So this does fit the generalization that evolution seeks paths that minimize energy expenditures.
Gregory & Mark–makes sense to me!
Thanks for the butterfly photos. Love how they contributed to such a robust and interesting discussion. But no anthropomorphizing this time 🙁 Hard to do w/ insects.
I know, right? I think that’s one reason I’m drawn to arthropods in general–one of the easy-to-encounter groups that yet seems so alien.
Though I’ve known a few hermit crabs that seemed a bit personable.
It’s entirely possible that some animal has urinated on the plant, and the monarchs are eagerly seeking the salt and minerals- this is a common sight in the woods; butterflies of all kinds attracted to animal urine.
So far as the mimicry is concerned, I wonder if the toxic compounds play any part in favoring genes that express the orange color?
Animal urine? Where’s the romance in that Jeffrey?
Watch a buck deer making a scrape (which he returns to frequently to urinate) and then sniffing with his mouth open to detect the scent of a possible conquest, you’ll see that “love is in the air”!
That’s no candle light and champagne dinner, but ya, its pretty sexy.
Yeah, isn’t that called something like a “gah” when cats do that? Especially if they’ve just sprayed and then sniff it, or sometimes just sniffing their own nethers. They open their mouths just a bit and breathe in all the vapours…Yuck would be our version.
Your comment drives home just how unobservant I was at the time (remarkable how the search for a Black-headed Gull can preoccupy one). I’d been thinking that the Monarchs were showing interest in this plant in general–i.e., in all the individuals growing up and down the causeway. I do seem to remember, though, that they seemed particularly interested in the one at my feet…
Of course, that could just mean that one Monarch attracts others…
As a non-biologist, my first thought is that maybe Batesian and Müllerian mimicry should be considered a single mechanism — something like “it’s advantageous for this species to look like another unpalatable species”, with no reference to whether the first species is palatable or unpalatable. (Then Müllerian mimicry is just the application of this principle to both species at the same time.)
I think there’s a legitimate distinction to be made between, on the one had, two unpalatable species converging on a common signal for their mutual benefit, and on the other hand, a palatable species exploiting an existing signal for its own unilateral benefit.
I was going to post something similar.
If toxic monarchs overlap the viceroys’ range, it seems like it’s the same selection pressure causing viceroys to mimic monarchs regardless of whether the viceroys are toxic.
There may be reciprocal pressure on monarchs to resemble viceroys, but then it just seems like another instance of the same process, running in parallel.
In both cases they converge on a common signal, but whether the relationship is exploitative is still useful for our understanding of how it happened historically, I guess.
Seems to me the selection pressure will be reciprocal only if both species are toxic. Why would an unpalatable species want to look like a delicious one?
Right. In the Viceroy/Monarch example (with Monarchs toxic everywhere, and Viceroys toxic only in some places) the selection pressure is reciprocal only in those places where both species are toxic. So the presence of the selection pressure on Monarchs depends on where you are.
But the selection pressure on Viceroys to look like Monarchs, it seems to Adam and me, is the same process everywhere, whether the Viceroy is toxic there or not.
I disagree (except in the trivial sense that all selection is “the same process”). Here’s why:
When a naïve bird eats a toxic Viceroy, it learns a lesson that applies to both Viceroys and Monarchs. Two species are protected for the price of one death.
When a naïve bird eats a non-toxic Viceroy, it learns the opposite lesson: these things taste good! So it will go on eating them until it happens to get a Monarch instead. Several individuals must die, including at least one of each species, to teach the bird the right lesson.
In other words, Müllerian mimicry reinforces the protective effect of mimicry, whereas Batesian mimicry dilutes it. Different degrees of protection means different selection pressure.
Or so it seems to me.
In Batesian mimicry, if mimics outnumber models, then the protection of appearance may become lost as predators don’t encounter noxious models often enough to learn to associate that visual with distastefulness. Not so in Müellerian mimicry. That’s a reason to distinguish between them. Both are forms of mimicry, though, so that is the general phenomenon.
I don’t understand this. It seems to me that in places where Viceroys consistently vastly outnumber Monarchs, then there’s essentially no selection pressure on Viceroys to resemble monarchs — as you say, the protection of appearance is lost.
But as far as I can tell, this should be the case whether Viceroys are toxic (Müllerian mimicry) or non-toxic (Batesian mimicry) — so it’s not a reason to distinguish between the forms of mimicry.
Where toxic Viceroys outnumber Monarchs, birds are still reliably learning to avoid both species. So it’s still to their mutual advantage to resemble each other, regardless of their relative numbers, so that one lesson protects both species.
Where non-toxic Viceroys outnumber Monarchs, that’s not the case. Birds learn the wrong lesson, and the warning signal becomes worthless.
Rather than relying on intuition, I decided to run some numbers.
Start with some assumptions: The average bird will eat 100 Viceroys+Monarchs in its lifetime. It will eat them until it hits a toxic insect, at which point it will no longer eat insects that look like the toxic insect. Viceroys either look identical to Monarchs, in which case eating a single Monarch will provide 100% protection to Viceroys; or different, in which case eating a Monarch provides no protection to Viceroys.
(These assumptions are obviously far too simple to directly apply to the real world, but maybe they are close enough to the real world to confirm or disconfirm our intuitions.)
I will consider 8 cases. Either Viceroys are toxic or non-toxic; either Viceroys look the same as Monarchs or different; and either the Viceroy and Monarch populations are the same size, or the Viceroys outnumber the Monarchs 99 to 1. In each of these cases, I provide a single number, which is the number of Viceroys eaten by the average bird.
same-size/non-toxic/different: 50
same-size/non-toxic/same: 1
outnumber/non-toxic/different: 99
outnumber/non-toxic/same: 63
same-size/toxic/different: 1
same-size/toxic/same: 0.5
outnumber/toxic/different: 1
outnumber/toxic/same: 0.99
(Hopefully I got all those numbers right! Let me know if you have questions about the math, or you think I got them wrong.)
1) The advantage of mimicry in reducing deaths by predation is very strong if the populations are the same size and Viceroys are non-toxic; negligible if Viceroys are toxic and vastly outnumber Monarchs; and moderate in the other two cases considered. In particular, if you consider the cases where there are 99x as many Viceroys as Monarchs, Batesian mimicry still provides a strong advantage but Müllerian mimicry provides almost no advantage (to Viceroys). This is not what I said before, and if I understand you correctly, it’s not what you thought the effect would be either.
2) In all cases considered, the Batesian numbers are very different from the Müllerian numbers. That seems like a sufficient reason to treat them differently, so I retract my suggestion that Müllerian mimicry should be considered just a special case of Batesian mimicry.
Thanks for all the comments & discussion, folks. I wasn’t online much yesterday as one of my d*gs was quite sick (he’s recovered, thankfully) so I’m late to the program.
I especially enjoyed your elaboration on mimicry, Jerry.