Monarch coloration, milkweed toxins, and predation by birds

This text is both a preamble and addendum to the “Monarch Fallout and A Predator Story” blog article posted recently by Brad Guhr of the Dyck Arboretum (republished below, with permission).

PREAMBLE
Predation by birds has been offered as the explanation for monarchs’ aposematic coloration. This contrasting orange and black color combination is thought to be a feature that effectively advertises the toxic cardiac glycosides (also called cardenolides) sequestered in the tissues of adult butterflies from the milkweeds consumed during the larval stage. This interpretation is strongly supported by the experiments and numerous analyses conducted by Lincoln Brower and his colleagues. Among these tests were feeding experiments with caged naïve blue jays. Young jays, that had never seen a monarch, would unhesitatingly eat one when it was first presented as a food item. Within a short interval, the jays would vomit up the monarch due to the emetic properties of the cardiac glycosides. A picture of this reaction is iconic (see “The Case of the Barfing Blue Jay“), having graced the pages of Scientific American and many a biology textbook. The jays thereafter refused to eat monarchs when presented among food items. This learning by experience, though some monarchs are consumed in the process, is said to provide monarchs, as a population, with a degree of protection from bird predation since birds, being highly visual, recognize the contrasting colors and, after a feeding experience, subsequently avoid feeding on monarchs or perhaps all species displaying these colors. Indeed, observations of birds feeding on monarchs, other than the black-backed orioles and black-headed grosbeaks that prey on monarchs clustered in the oyamel fir trees in Mexico, are rare.

Yet, now and then, we hear of instances in which observers have reported seeing scissor-tailed flycatchers and Mississippi kites feeding on monarchs during the migration. Unlike blue jays, that stopped eating monarchs after one experience, the scissor-tails and Mississippi kites appear to be undeterred by the cardiac glycosides in the monarchs. Still, the stories that reach us have always been fragmentary. The following blog article created by Brad Guhr, of the Dyck Arboretum, in Hesston, KS, and the wing collection assembled by Karen and Dick Fulk, describe an instance of intense predation by 5 immature Mississippi kites on migratory monarchs that had taken temporary shelter within the grounds of the arboretum.

Monarch Fallout
It happened again in 2020. The convergence of the peak of the September monarch southerly migration over Southcentral Kansas was met by a strong south wind, causing a “fallout” of monarchs at the Dyck Arboretum. Rather than waste energy fighting the headwind, monarchs find a place of refuge to rest and sip nectar. I would estimate that I’ve seen this phenomenon happen five times in the Arb since 2005 and this year’s was the most memorable for a few different reasons including big numbers, fallout location, and a predator story.

Monarchs in the Hedge Row at Dyck Arboretum, 9/20/2020 – Photo by Gerry Epp

Big Numbers
The monarch numbers I observed on Monday, 9/21/2020 seemed to me to be more stunning than I can ever remember. I estimated conservatively in a report to Journey North, there were at least 500 monarchs resting in the Arboretum that day. But after giving it more consideration and talking to a local monarch tagger, Karen Fulk, I wonder if that number was more accurately in the thousands.

Karen’s many years of efforts to tag monarchs in Hesston has her keenly in touch with monarch phenology and migration patterns. She reports that the peak of migration through south central Kansas is usually between 9/22 and 9/27. This year, however, she started seeing an uptick in numbers when a cold front and north wind jump-started the southerly monarch migration a bit earlier.

Karen usually tags 300 annually during the fall migration. This year, Chip Taylor at Monarch Watch, knowing that migration numbers were higher this year, suggested that Karen start with 500 tags. She was able to apply most of those 500 tags when the fallout began Friday 9/18/2020 through Sunday 9/20/2020. Arboretum member, Gerry Epp, further documented this event by posting photos of the fallout on his Facebook page, 9/20/2020.

Monarchs on Seven Son Flower at Dyck Arboretum, 9/20/2020 – Photo by Gerry Epp

Fallout Location
With some repetition now in seeing these fallouts occur in the same place, I want to give some thought to why they congregate where they do at Dyck Arboretum. Karen usually tags at three places in Hesston based on the ability to catch and tag the maximum number in one place, and Dyck Arboretum is where she does the majority of her work. She estimated that 95% of her tagging this year happened at the Arboretum, based on seeing the greatest number of butterflies here.

I would hypothesize that they repeatedly congregate in the small 1/8th-acre area at the Arboretum amphitheater/pinetum for three reasons. One, they are seeking protection from the elements of wind and heat. This is about energy conservation. By escaping the wind and congregating in large groups on the north side of the dense hedge row of Osage orange trees, they are finding a microclimate that is cooler, more humid, and less turbulent than they would find on the south side.

Monarchs on Seven Son Flower at Dyck Arboretum, 9/20/2020 – Photo by Gerry Epp

Two, this location is next to a number of nectar sources. Why not rest where you can eat/drink too? Nearby native plant beds and a reconstructed prairie had a timely profusion of flowering from many species of the genera Helianthus (sunflower), Solidago (goldenrod), Symphotrichium (aster), Liatris (gayfeather), Eryngium (eryngo), and Heptacodium (seven son flower).

Three, a number of white pines in this location may resemble the trees of the Oyamel fir forests in Mexico. I don’t have any proof of this theory, but it seems plausible to me.

Predator Story
The newest wrinkle of this monarch fallout experience was the side story of five immature Mississippi kites. They were probably migrating with the monarchs and decided also to not fight the strong south wind. For a day and a half that I observed, this hungry bunch of pentomic predators took advantage of an abundant food supply. They hung out in the top of one of the white pines and took turns swooping through the monarch clouds to easily catch a snack.

Mississippi Kite Eating A Monarch at Dyck Arboretum, 9/22/2020 – Photo by Janelle Flory Schrock

Sometimes they missed catching their target, but usually, these agile insect catchers snagged their prey. Typically they would return to their perch to eat their catch, but sometimes they would eat in flight or “on the wing” as I hear experienced birders say. At one point, I counted approximately 120 monarch wings that had fluttered down to form what I’ll call a monarch confetti debris field. At four wings per monarch, that represented the carnage of about 30 monarchs. However, a number of wings had already been collected by onlookers, so it is not unreasonable to think that the number of monarchs preyed upon were double or triple what I saw.

Monarch Wings at Dyck Arboretum, 9/20/2020 – Photo by Brad Guhr

Monarch Toxicity
This predator behavior was a surprising observation. Monarch larvae eat milkweed and sequester in the mature butterfly wings and exoskeleton the milkweed toxins called cardiac glycosides. These heart poisons can seriously affect vertebrate predators, including birds, and often cause them to vomit and subsequently avoid eating them further. However, these young kites not only ate monarchs all day Monday, but they continued their feeding frenzy the next morning. Either their stomachs weren’t too adversely soured, or the calories needed to continue this migratory journey were simply too important.

A Google literature review turned up no articles mentioning this habit of Mississippi kites eating monarchs. However, a follow-up conversation with University of Kansas Professor, Brad Williamson, helped me understand that this observation is not so irrational. He explained that the monarch population is not 100% toxic.

“The individual toxicity depends a lot on the particular milkweed species that hosted the larval stage. Asclepias syriaca (common milkweed) and Cynanchum laeve (honeyvine milkweed) are not nearly as toxic as A. verticillata (whorled milkweed). There is an entire range of toxicity and it makes for some great mathematical modeling questions–just how much toxicity (percent toxic) in the population is necessary for protection for the entire population? How much metabolic costs are there for monarchs trying to process highly toxic host plants? Turns out that only 25-40% of the population being toxic confers protection for the remaining population.” (I will include below a bibliography on monarch toxicity that Dr. Williamson provided if any of you are interested as I am in learning more about this topic.)

There were a lot of interesting biological and ecological issues at play here with these monarchs and kites. It was just one more interesting natural history story with subplots to be observed by those of us living in the Monarch Flyway. Until I’m able to one day witness the hundreds of millions of monarchs wintering in the the Oyamel forests of central Mexico, I am completely content having a front row seat to this fascinating migration phenomena right here in Kansas.

Plant Milkweed
To assist the monarchs and their annual migration, plant milkweed host plants and other native nectar plants for adults. Check out our annual spring and fall Flora Kansas native plant sales.

Articles on Monarch Toxicity
Brower, L. P., and C. M. Moffitt. “Palatability Dynamics of Cardenolides in the Monarch Butterfly.” Nature 249, no. 5454 (1974): 280–283.

Brower, Lincoln P. “Avian Predation on the Monarch Butterfly and Its Implications for Mimicry Theory.” The American Naturalist 131 (1988): S4–S6.

Brower, Lincoln P., and Susan C. Glazier. “Localization of Heart Poisons in the Monarch Butterfly.” Science 188, no. 4183 (1975): 19–25.

Brower, Lincoln P., Peter B. McEvoy, Kenneth L. Williamson, and Maureen A. Flannery. “Variation in Cardiac Glycoside Content of Monarch Butterflies from Natural Populations in Eastern North America.” Science 177, no. 4047 (1972): 426–429.

Fink, Linda S., and Lincoln P. Brower. “Birds Can Overcome the Cardenolide Defence of Monarch Butterflies in Mexico.” Nature 291, no. 5810 (1981): 67–70.Malcolm, S. B., and L. P. Brower. “Evolutionary and Ecological Implications of Cardenolide Sequestration in the Monarch Butterfly.” Experientia 45, no. 3 (1989): 284–295.

Malcolm, Stephen B. “Milkweeds, Monarch Butterflies and the Ecological Significance of Cardenolides.” Chemoecology 5, no. 3–4 (1994): 101–117.

Malcolm, Stephen B., Barbara J. Cockrell, and Lincoln P. Brower. “Cardenolide Fingerprint of Monarch Butterflies Reared on Common Milkweed, Asclepias Syriaca L.” Journal of Chemical Ecology 15, no. 3 (1989): 819–853.

Nelson, C. J., J. N. Seiber, and L. P. Brower. “Seasonal and Intraplant Variation of Cardenolide Content in the California Milkweed, Asclepias Eriocarpa, and Implications for Plant Defense.” Journal of Chemical Ecology 7, no. 6 (1981): 981–1010.

Roeske, C. N., J. N. Seiber, L. P. Brower, and C. M. Moffitt. “Milkweed Cardenolides and Their Comparative Processing by Monarch Butterflies (Danaus Plexippus L.).” In Biochemical Interaction between Plants and Insects, 93–167. Springer, 1976.

Zalucki, Myron P., Lincoln P. Brower, and Alfonso Alonso-M. “Detrimental Effects of Latex and Cardiac Glycosides on Survival and Growth of First-Instar Monarch Butterfly Larvae Danaus Plexippus Feeding on the Sandhill Milkweed Asclepias Humistrata.” Ecological Entomology 26, no. 2 (2001): 212–224.

The post Monarch Fallout and A Predator Story appeared first on Dyck Arboretum.

ADDENDUM
Karen Fulk had been tagging monarchs in the area at the time of this event, and wings of seven of her tagged monarchs were found among the scattering of wings in the area of intense feeding by the Mississippi kites. Curious to learn more, Karen made a search for all the wings she could find. She collected many, but some were evidently collected by others. Still, the collection gives us a rough idea of the total number killed and the sex ratio of those consumed.

Karen gave a quick look at the wings and concluded that the sample represented over 90 monarchs. Since it was of interest to determine the sex of each forewing to determine the sex ratio of the sample, Karen being less certain of those determinations, sent the collection to me.

The results of sorting the wings by sex and left verses right are given below.

This tabulation suggests that AT LEAST 50 females and 43 males, or 93 in total, were killed and eaten by these birds while the monarchs were roosting in and passing through the arboretum. It would seem that the cardenolides had minimal effect, if any, on the feeding habits of these Mississippi kites. Curiously, I saw no signs of beak marks on any of the wings.

Bag of monarch forewings

Left and right female monarch hindwings

Hindwings of tagged monarchs eaten by Mississippi kites at the Dyck Arboretum 21-22 of September 2020.