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The Many Disguises of the Passion Flower, Passiflora
Passiflora, a big tropical genus
The way plants relate whether to its adversaries (plants and animals) or their allies (e.g. pollinators, seed dispersers) never seizes to amaze me. Chemistry is their most frequent weapon of choice and quite often it serves plants well in detracting their most feared herbivores enemies. However, as amazing as it can be in some very well-known cases, for the most part the Game of Thrones happening at every second of every day in the plants that surrounds us is mostly unknown and most of all unnoticed. Among the very well studied cases, there is one that stands out particularly not only by the fact that it shaped the evolutionary history of its main characters (plant and animal species) but also the lengths taken the plant in order to avoid being eaten and extinguished. Before dealing with the intricacies, the violence and ironically the passion of such relation let us first learn a bit about the plant in this story, the famous passion flower, Passiflora.
Passiflora is genus of more than 530 species of flowering plants, mostly vines and a minority of bushy or herbaceous species, and is the main genus of the family Passifloraceae. Passiflora macrophylla is one of the few exceptions as it can grow up to what one can call a small tree, up to 6 m tall with its gigantic leaves. This number is likely to increase as new species have recently been found. Passiflora species are found in all tropical regions of the globe except in Africa but they are mostly concentrated in South America, especially in northern Brazil. Many are grown as ornamentals due to their famous, very complex and unusual flowers – the passion flowers. The fruits of Passiflora are all edible, however not all particularly attractive for our human taste. Very few species are grown for their fruits and the most important commercially is Passiflora edulis which is grown for its fruit (passion fruit). Other species grown for their fruits include: Passiflora ligularis; Passiflora incarnata; Passiflora quadrangularis; Passiflora foetida; Passiflora tripartite; and Passiflora tarminiana. From many of these species, as well as from those grown for ornamental purposes only, many cultivars and hybrids have been developed whether to obtain tastier fruits or different and unusual flowers. Some species, e.g. Passiflora incarnata, have also long been used by local natives in traditional medicine due to the rich chemical arsenal found in its leaves. What stands out the most of these plants is their very beautiful and complex fragrant flowers with a unique structure adapted in most cases to a particular pollinator species. Usually there are effectively pollinated by large bees, e.g. bumble bees, beetles, wasps, moths, butterflies, humming birds and even bats.
Northern South America, where most Passiflora species exist
The Flower of the Passion of Christ
The unusual aspect of Passiflora flowers, passion flowers, is the reason for its popular and scientific names. Spanish Jesuits exploring South America, at the time known ad New Spain, at the beginning of the seventeen century were particularly impressed by their unusual appearance. On describing the plant, namely its flower parts and their number they associated these exotics plants with the last days of Jesus and especially his crucifixion – the Passion of Christ. The Jesuit priests who first described the Passiflora genus, named these species as “la flor de las cinco llagas" (the flower of the five wounds). The first specimens of Passiflora and descriptions of some species were sent to Rome in 1609 as a gift to Pope Paul V. Giacomo Bosio, brother of the Order of St. John of Jerusalem and historian, interpreted the flower parts from drawings and dried plants as representing various elements of the Crucifixion naming the flower passiflora. The pointed tips of the leaves were taken to represent the Holy Lance and the tendrils the whips used in used in the flagellation of Christ. The petals and sepals, usually ten, were taken to represent the ten faithful apostles (excluding Peter the denier and Judas Iscariot the betrayer). The flower’s filaments, which can vary between flowers in color and number (in some cases hundreds, e.g. Passiflora edulis) represented the crown of thorns. The chalice-shaped ovary with its receptacle represents a hammer or the Holy Grail. The three stigmas (female organs) were taken as the three nails (one for each hand and one for the feet) and the five anthers below them the five wounds (four by the nails and one by the lance). Finally, to give a more sacred and heavenly touch, the dominant blue and white colors common in the flowers of many species were considered to represent Heaven and Purity. The idea and the inspiration remained until today where these plants are known popularly in many languages (with Christian tradition) by names whether associated to the Passion of Christ, the wounds or the crown of thorns.
Due to their elaborate and complex chemical arsenal, there are not many animals that eat Passiflora leaves. In fact, the biggest threat to Passiflora vines comes from butterflies, namely those from the genus Heliconius. These butterflies have evolved the ability to circumvent the chemical defenses of Passiflora so successfully that they only deposit their eggs on Passiflora species. In some cases, some Heliconius species deposit their eggs in one Passiflora species only; e.g. in Costa Rica Heliconius hewitsoni is totally dependent on Passiflora pittieri. On the other hand, the females of Heliconius cydno lay their eggs on many different species of Passiflora. There is a small number of other insects that also deposit their eggs on some passion flower vines, e. g. flea beetles, flag-legged coreid bugs. However, none of these insects is as dependent on Passiflora species or skilled as Heliconius butterflies at finding new shoots on mature vines or at finding isolated juvenile vines. The larvae of Heliconius are so voracious that they threaten the life of Passiflora vines, even adult plants. A single Heliconius caterpillar can easily consume all the leaves of a juvenile vine during its lifetime. The surviving of such dramatic defoliation event will certainly slow the plant’s rate of growth at a critical time in its life cycle. For this reason Passiflora species have evolved a set of strategies to detract such pests. Ironically, some Heliconius species can occasionally pollinate some Passiflora species.
One of the most common defense strategies from Passiflora species is the development of small colored nubs on young leaves and shoots mimicking the yellow Heliconius eggs. These egg-like structures are slightly modified nectar glands and their main function is to fool Heliconius butterflies into thinking that there are already too many eggs deposited on this particular part of the plant so that the larvae of this supposedly “late” butterfly mum will have fierce competition of some other’s progeny. To help this con and present a more realistic scenario Passiflora vines also delay the development of the parts presenting these fake eggs giving the idea that possibly these parts are not that young and yummy as Heliconius might think. Or, if growing is really necessary, the expanding young leaves keep their growing (thus softer) tips hidden to prevent the visit of caterpillar or butterflies. This strategy serves well Passiflora as Heliconius being totally dependent on it are rather picky on choosing the best places to lay their eggs. Also, Heliconius caterpillars are aggressively cannibalistic both towards other younger caterpillars and eggs. Therefore, better not to take the chances on a leaf already “decorated” with possible menaces. Alternatively, other species of Passiflora, e.g. Passiflora pinnatistipula, present modified nectarines that mimic the eggs of predators which might eat the eggs of Heliconius. The problem for Passiflora vines then becomes deciding how many fake eggs one has to produce in order to fool a Heliconius butterfly.
To increase the chances of not being eaten by voracious caterpillars or if the fake eggs that they present are not that convincing, Passiflora species also developed the habit of presenting drooping growing tips and shoots giving the idea that they are wilting or sick. Therefore, these plants seem to be not in such good conditions, possibly not being able to serve as food or even live enough in order to assure caterpillar’s life cycle. Again, Passiflora takes advantage of the picky nature of Heliconius butterflies on choosing the best plants to lay their eggs; i.e. young, green and turgid full of vigor. In addition, Heliconius have a mind set of what a leaf of a healthy Passiflora vine should be. This is important as being totally dependent on these plant species for survival it is important for Heliconius to distinguish from all the surrounding plants where Passiflora species are; especially when these are not flowering. Here comes (in my opinion) one of the most ingenious strategies of Passiflora, that is changing leaf shape. Heterophylly (presenting different forms of leaves in the same plant or during different stages of development) is not specific of Passiflora species. In fact, is quite common in many plant species, e.g. eucalyptus, carnivorous plants. But none takes to the extent that Passiflora does. If we could name a chameleon in the Plant Kingdom, that would be Passiflora. The extent and diversity of leaf shapes and changes seems endless and it varies between Passiflora species and the pressure that they suffer from Heliconius species on a given location. Passiflora vines change the number of lobes from their normal palmate five lobe shape, whether increasing it or decreasing it. They change the leaf shape altogether, for example presenting ovate (oval with no lobes) leaves with entire or serrate margins. These changes can occur between juvenile and adult stages of development or between different parts of the plant. The main goal is, as always, to trick Heliconius butterflies that they are possibly laying their eggs on the wrong plant even if that plant has flowers similar to Passiflora. To add to their disguising skills Passiflora species may also present infrequent shoot development in order to confuse the butterflies on when to look for new growing plants. Unfortunately for Passiflora species, Heliconius adults can live up to nine months which gives them quite some time to wait for new shoots to develop.
As a third set of elaborate maneuvers to detract Heliconius butterflies, many Passiflora species, e.g. Passiflora incarnata, produce sweet nutrient-rich nectar from extra-floral nectaries on stems and petioles. This seems to attract ants which defend the plant by killing and eating many competitors or pests that they happen to find feeding on the passion flowers, including Heliconius caterpillars. Also, not being on the flowers these nectarines keep the ants distracted from them allowing pollinators to do their job undisturbed. Other type of adaptations taken by some Passiflora species, e. g. Passiflora adenopoda and Passiflora lobata, is presenting modified trichomes (epidermal hair or scale like outgrowths on plant foliage) in the form of hooked hairs that entrap caterpillars causing their death. But, perhaps the most extreme defense mechanism comes from Passiflora foetida, the stinking passion flower, as it is able to trap insects on its modified bracts. The bracts exude a sticky substance that also contains digestive enzymes. It is thought that this mechanism minimizes predation on young flowers and fruits. However, the benefits and gains as nourishment from its “prey” are yet to be determined. Passiflora foetida is thus considered a protocarnivorous plant.
Ants feeding on extrafloral nectaries of Passiflora
Finally, one should note that all these mechanisms and adaptations are mostly due and are especially observed when Passiflora species feel high pressure from herbivores. On the other hand, the defenses put by Passiflora species put pressure on Heliconius and other insect species that feed on Passfilora plants to evolve and circumvent these defenses. As being adaptable as passion flowers are it is thus no surprise that your exotic passion flower at home does not present any of these curious adaptations, especially when they have nothing to fear from. Well, basically this is what my Passiflora caerulea does by sitting under the sun while happily growing and flowering, thus far from being the 007 of the Plant Kingdom here described.
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