The Drama of Milkweed Pollination

Craig Holdrege

From In Context #23 (Spring, 2010)

With a special focus on the remarkable sequence of events resulting in the pollination of the milkweed flower, this article one part of a more intensive study by Craig, with illustrations and photos, of the complex life story of milkweed, “The Story of an Organism: The Common Milkweed.” The full study also depicts how an organism always leads beyond itself to a larger web of relations with other organisms and elements of the environment.

When you see an old field, the robust common milkweed plants stand out among the much sleeker grasses, asters, or goldenrods. Common milkweed has thick stems and expansive leaves that, in shape and size, look more like the leaves of a plant growing in shady woods than in a sunny old field. In the warm summer days of late June and through much of July, the large spherical heads of flowers unfold on the upper part of the stems. The individual flowers are actually quite large for a field plant and they produce large amounts of concentrated nectar. Their scent spreads out into the surroundings. When in flower, a colony of milkweeds attracts — day and night — a great variety and number of insects of all different shapes and sizes. For several weeks in summer milkweed becomes a microhabitat with a singular concentration of insect life.

After the flowers wilt, the fruit pods begin to expand. While relatively few fruits form out of the multitude of flowers, those that develop grow large — much larger than those of other old field community plants. The pods swell and orient themselves upward, a contrasting gesture to the globes of flowers. Each pod is full of seeds, seeds that are large and heavy. But they have the light feather-like extensions of the white comas that allow them to be carried away on a breeze when the pods split open. It is almost as if the upward pointing pods are prefiguring what is to come — the upward lift of the coma-bearing seeds that disperse into the larger environment. As with all stages of milkweed, both pods and seeds provide nourishment to insects.

One salient feature that informs milkweed is its exuberant and robust growth. Underground it spreads year to year, forming a network of thick rhizomes out of which the above-ground shoots grow. The thick shoots bring forth large, spreading leaves. All these parts of the plant contain the milky sap, which is continually produced as the plant grows and develops. A marked transformation in substance and form occurs as the many large umbels (flower clusters with all the flower stalks originating at the apex of their common stem) unfold in the summer light and warmth. As the stems and leaves are rich in milk sap, so are the flowers rich in sweet nectar.

Flower Morphology and Pollination

While the form of the leaves in common milkweed — and other members of the genus as well — is simple and the shape hardly transforms from bottom to top of the stem, the flowers are highly complex and differentiated. It took a good deal of detailed botanical study to identify and relate milkweed flower structure to the anatomy of other flowers.

Then the flower opens, five small green sepals fold back and then five larger elliptical white to pink petals also fold back and come to lie more or less parallel with the flower stalk. In most “typical” flowers of other kinds of plants you find the circle of petals surrounding a circle of stamens, whose anthers release pollen, and then in the center of the flower the pistil in which the seeds will develop. Neither the pistil nor the stamens are clearly recognizable in the milkweed flower. Rather, a number of accessory organs form out of the partially fused stamens and pistil.

Figure 3 gives a diagrammatic representation of the milkweed flower. Above the petals is a so-called corona consisting of five cuplike hoods out of which extend little curved horns. The hoods hold the nectar that attracts so many insects on warm, sunny summer days. In between the hoods are little vertical slits. Each slit opens into a stigmatic chamber. (What it has to do with the stigma, we will see further below.)  Above the slit there is a tiny black knob, the corpusculum. What one doesn’t see is that the corpusculum has two little arms (called translator arms) that extend into the two upper sides of the chamber. Each arm attaches to a golden package of pollen, called a pollinium. Each of the pollinia houses hundreds of pollen grains. Unlike the pollen in most flowers, which is released from the anthers while they are still attached to the flower, in milkweeds the pollen remains contained within the pollinia until it comes in contact with the stigma of a flower. Only orchids — also plants with complex flowers — package their pollen in a similar way.

The only way for the pollinia to escape their chambers is via insects. As already mentioned, milkweed flowers are visited by amultitude of insects in search of nectar — which they find in generous supply. Not only is the nectar very rich in sugar content, being up to 3% sucrose, but the supply is also renewed over the life of the individual flower. Milkweed flowers produce much more nectar than the many insects feeding on it could ever remove.

While the insects are moving around on a flower — they sometimes go from hood to hood on a single flower — one of their legs may slip into a slit. I have often observed honey bees and flies struggling to pull a leg out of the slit. Most often it succeeds by pulling its leg upward whereby the leg hooks into a groove on the corpusculum at the top of the slit, and as a result the insect pulls the whole pollinarium — corpusculum,  two translator arms and two pollinia — out of the stigmatic chamber.

One study showed that a bumble bee picks up on average a new pollinium every 2 to 5 hours and that the same pollinium remained attached to the legs for on average 2.5 hours, while if attached to the mouthparts, the pollinium stayed attached for 10 hours. As an insect continues its nectar foraging, it often accumulates multiple pollinaria. One pair of researchers reported finding up to 35 pollinaria on a single insect; sometimes they are hooked together in chains of ten or more dangling from an insect’s leg. Most often one sees honey bees (Apis mellifera) with many pollinaria attached to them (Figure 4b).

Smaller insects — I have observed mainly flies — may be unsuccessful in removing a leg from a slit and the limb will tear off in the process. I have also seen dead flies hanging from a flower with a leg still caught in a slit. Larger pollinators like bumble bees and honey bees are more likely to extract pollinaria without losing a body part.

What happens to the pollinaria? Many will simply drop away or be rubbed off as the insect moves around. A few will find their destination in another flower. And just as the removal of the pollinaria is both a haphazard and narrowly constrained process, so also is pollination. First, something remarkable and absolutely essential for pollination occurs with the pollinarium itself. After an insect has been carrying around a pollinarium for about ninety seconds, the pollinarium dries out and in the process the translator arms rotate ninety degrees. This torsion is highly significant because it brings the pollinium into a position that allows it to slip into a slit when an insect moves over one. Before the torsion, the broad side of the pollinium usually faces the slit as the insect crawls along; afterwards the narrow side of the pollinium is in line with the slit so that if the insect is moving at just the right height over a slit, the pollinium can slide into the stigmatic chamber. As the insect moves ahead, the translator arm breaks and the pollinium remains behind. Once in the chamber, one edge of the pollinium rests against the receptive wall of the stigmatic chamber. While in most flowering plants the stigma is open to direct contact with the air and visiting insects, the five receptive stigma surfaces in milkweeds are enclosed within five stigmatic chambers, open to the world only through the narrow slit. So in milkweed flowers both pollen grains and stigmatic surfaces are housed in enclosed structures.

Only when the pollinium slides into the stigmatic chamber can this encapsulation be overcome. Everything I will now describe is visible only when one dissects flowers at different stages of the pollination process and looks at the structures under a microscope. The stigmatic chamber is the source of nectar for the hoods, and when the pollinium is inserted into the chamber it is bathed in nectar and begins to swell. Within a few hours the edge that is in contact with the receptive inner surface of the stigmatic chamber breaks open and multiple pollen tubes grow out of the pollen grains. The tubes grow down the style and into one of the two ovaries of a flower. An ovary contains a couple of hundred ovules and each one needs to be fertilized by the nucleus from one pollen tube. Interestingly, when fertilization occurs, virtually all the ovules are fertilized — one rarely finds milkweed pods with just a few seeds.

One could at first think that the highly specialized pollination apparatus, which provides a seemingly perfect fit between pollinium and stigma, would guarantee successful fruit set. But this is not the case. In the first place, the specialization also means that relatively few pollinia actually are successfully inserted into a stigmatic chamber. Secondly, researchers discovered that common milkweed is self-incompatible. This means that the pollinium from a flower that is inserted into a flower of the same colony will normally not bear fruit. The pollen tubes grow into the ovary but the seeds do not develop. Because insects are moving largely within a given colony, it is likely that most of the pollinia inserted come from flowers of the same colony and will therefore not lead to successful fruit set. One study using radioactively labeled pollinia found that a third of the pollinia inserted were from the same umbel and most of the other inserted pollinia came from the same colony; only a few were carried to other colonies and successfully inserted.

As if this “inefficiency” — we could also call it over-abundance — were not odd enough, even when researchers cross- pollinated flowers of related Asclepias species by hand, fruit set never exceeded 20% and was usually considerably lower. Thus, overall, the specialization of milkweed pollination, at least in relation to successful fruit formation, is connected with a low vitality. If one looks, however, at a milkweed colony from the perspective of the many insects that feed on the flowers’ nectar, milkweed is contributing significantly to the vitality of those animals. Of course, the picture is more complex if we think of the occasional death of mainly smaller insects unable to remove a limb that has been caught in a slit.

One interesting feature of the relation between flower structure and insects is that although all milkweeds have such specialized flowers, they are visited by and can be pollinated by a wide array of insects. The nectar also attracts ants and small beetles that usually contribute little toward pollination, but reap the benefits of the ample nectar supply.

Milkweed's highly specialized flowers and the intricate pollination process bring into focus how an organism extends beyond itself through its relations to insects in its environment. And as we will see in a subsequent essay, the story of the relation between common milkweed and insects is even more complex: a number of insect species and common milkweed have co-evolved, resulting in the insects becoming so specialized that their lives are inextricably intertwined with the plant.

References

References can be found in the full-length article on common milkweed, posted here.