Shape Shifters
Scott Zona, Ph.D., Former Palm Biologist
“It's not easy being green” Kermit the Frog famously observed. His introspective comment applies to plants as well as amphibians. As if it were not hard enough finding a place to grow, a green plant has to rely on the vagaries of rainfall and soil fertility and the fick1e nature of pollinators and seed dispersers, to say nothing of herbivores and the competition. There are allies and adversaries out there, but which is which? No, Kermit, it's not easy being green.
Passion vines, members of the genus Passiflora, are not exempt from Nature's struggle for existence. They share Kermit's complaint, but they have, nevertheless, succeeded in some pretty spectacular ways. Passiflora is a tremendously diverse genus of some 500 species, ranging from delicate annuals to tree-toppling woody lianas to fully self-supporting trees. Most climb with twining tendrils, but a few have branched tendrils tipped with sticky pads. The trees have no tendrils at all.
Passion vines are most abundant in the rainforests of northern South America, but a few species venture as far north as the Midwestern U.S., while others have found their way to Australia and islands in the Pacific. We have a small number native to Florida, and one or two introduced weeds. There are three or four species commonly encountered in the gardens of South Florida, but those in cultivation are but a fraction of the diversity for which the genus is justly famous.
The Passion Flower Legend
Who among us has not heard of the legend of the Passion Flower, Passiflora incarnata? The spiky purple-blue flowers were said to have been used by early Spanish missionaries to exemplify lessons from the Passion, or Crucifixion, of Christ. The ten sepals and petals represent the ten true Apostles, the spiky crest represents the crown of thorns, the five stamens represent the five wounds, and the stigmas, the three nails. Whether one's interest in the flowers is theological or horticultural, there's no denying that the flowers are strangely beautiful. Nevertheless, it is worth remembering that the flowers are not produced for the conversion or diversion of our souls. They are, subversively enough, for sexual reproduction. Seventeenth century missionaries would have been scandalized.
Floral Diversity
The flowers of Passiflora are intricate and even bizarre, but all of their structures can be matched with the “typical” parts of a flower: sepals, petals, stamens, and pistil. In Passiflora, the sepals and petals are usually similar in size, shape and color and are collectively referred to as tepals. The tepals are fused together at the base to form a shallow cup that holds nectar. From the base of the tepals arises a passion flower's most distinctive finery, a whorl of spike filaments called the corona (Latin for “crown”). The corona seems like a completely new addition to the basic flower plan until we realize that it is just an outgrowth of the tepals. In the center of the passion flower, the stamens and pistil are borne on a stalk that elevates them above the nectar cup. There are five stamens, and the pistil has three stigmas.
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| The corona is an outgrowth of the tepals of Passiflora incarnata, the maypop, a drought-tolerant species native to the Southeastern United States. | Passiflora perfoliata, a hummingbird-pollinated species from the Caribbean. |
In the case of Passiflora flowers, the floral parts have been molded by evolution so that differences in size, color, and posture accommodate the services of different pollinators. The blue, purple or rose flowers with spreading tepals and corona illaments are attractive to bees. But change the color to red, allow the flower to hang downward, draw the tepals forward and fuse the corona filaments to form a tube, and you have a flower that is attractive to hummingbirds. Make the flowers pale green and nocturnal, give them a musty scent, and the flower attracts nectar-feeding bats. These kinds of changes have happened over and over again within the genus. Bee pollination is believed to be the ancestral condition in Passiflora. A dozen separate lineages have evolved to be pollinated by hummingbirds, while three different lineages have evolved to be pollinated by bats. Shifts in ecological niche or strategy allow passion vines to occupy and exploit new territory. The change is a lateral shift from one pollination strategy to another, allowing a new guild of pollinators to be drafted into service of the Passiflora. A new flower form may be preferentially visited by a certain pollinator, resulting in abundant seed set and the passing of genes to the next generation, perpetuating the new form. This is one way in which new species form.
Leaf Diversity
Floral diversity is equaled by leaf diversity. Passiflora leaves come in a variety of shapes and sizes. Most commonly, they have two or three lobes, or they may have striking patterns on their leaves. Passiflora trifasciata has three-lobed leaves mottled with pink, the undersides of which are rich purple. Our native Passiflora suberosa is an over-achiever when it comes to leaf diversity. One can find several different leaf shapes in this species, from lobed to lance-shaped, broad to narrow, smail to large. In fact, all of these different shapes can be found on a single individual!
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| These leaves of Passiflora suberosa were taken from just one plant! Its diverse leaf shapes are as confusing to butterflies as they are to people. | The purple and pink leaves of Passiflora trifasciata, here growing among Hoya australis, are more colorful than the flowers, which are white. | Extrafloral nectaries are visible as tiny yellow spots on the leaves of Passiflora billora. |
Why do passion vines of the same species produce leaves of different shapes? Does periodically changing shape confer some advantage to the plants? Are vines that produce leaves of just one shape somehow disadvantaged? To learn the answers to these questions, we need to know about the behavior of the passion vine's arch enemies, butterflies of the family Heliconidae. Our native zebra longwing butterfly (Heliconus charitonius) is one of several hundred species that occur in the American tropics. Their larvae (caterpillars) feed on just one kind of plant: Passiflora. Butterflies find food plants on which to lay their eggs by using their eyesight and by tasting/smelling chemicals given off by the leaves. They “taste” the leaves by alighting briefly and touching the leaves with chemoreceptors in their legs or antennae.
Biologists have found that visual cues are almost as important as chemical cues, and that passion vines can sometimes escape detection from butterflies by looking like other nearby plants. In other words, the chameleon shapes of Passiflora leaves will occasionally blend in with the rank growth of surrounding vegetation, and gravid butterflies will lay their eggs elsewhere. The camouflage pays off just often enough for the Passiflora to reproduce. Score one for the Passiflora.
Passiflora also has another defense. Examine a passion vine and you'll find spots or glands on their leaves, on the petiole, or on the bracts (modified leaves) found below the flowers. These spots are extrafloral nectaries. Nectaries are nectar-producing glands; they are “extrafloral” because they are found outside the flower, which is where nectaries are usually found. Extrafloral nectaries play an important role in a symbiotic relationship that defends passion vines from insect predators, including the larvae of Heliconidae butterflies. The nectar that passion vines secrete attracts ants, as sugar inevitably does. The mercenary ants, in turn, are aggressive defenders of their food sources and will kill or drive off herbivores that would eat those sources. Thus both parties benefit from the relationship.
The conspicuous extrafloral nectaries on the surface of the leaves have another function: Because they resemble butterfly eggs, they are a visual deterrent to gravid female butterflies that might be searching for a place to lay their eggs. Here's how it works: Gravid females search for suitable leaves on which to lay their eggs. They look for leaves of passion vines that are large enough to provide a good meal for their offspring, and they look for leaves that are not already occupied by another female's eggs. The extrafloral nectaries on the leaves look enough like eggs to fool mama butterfly into thinking that the leaf is occupied, so she takes her eggs elsewhere. It doesn't work every time, but it works often enough to allow the passion vines to flower and reproduce.
Passion vines also rely on toxins to escape the predation of insects. Passiflora species produce cyanide compounds in their leaves and stems. When a insect takes a bite out of a Passiflora leaf, it gets a mouthful of cyanide and an upset stomach, a not-so-gentle reminder that the vines are not all-you-can eat buffets. Cyanide is a good defense against most insects, but Heliconidae butterflies have the ability to detoxify the cyanide compounds and store the cyanide in their own bodies, which deters birds from eating them. The caterpillars feed on Passiflora with impunity and purpose. Advantage: caterpillar.
The diversity of flower and leaf shapes in passion vines may appear profligate, but in fact, evolution is conservative in the way it manufactures diversity. What appear to be novelties are in fact cobbled together from existing parts. The corona is an outgrowth of the tepals. Leaves are recast as nectaries, which are reshaped to mimic insect eggs. Bee-pollinated flowers are retooled to attract hummingbirds. Structures are reshaped, but nothing is created de novo. Evolution works by modifying pre-existing structures, chemicals, or ecological strategies and reshapes them to function in new ways. The driving force behind these changes is the struggle for survival — Kermit's complaint — and the arms race between Passiflora and its butterfly enemies. This is how diversity arises in nature. It challenges all botanists to understand where, why, and when the changes occurred. In Passiflora, we have our work cut out for us: It will keep the botanists busy for a very, very long time.
Garden Views Autumn 2002