The Clever Lever

Since early times Salvia has been related to healing problems in human health; its very scientific name derives from the Latin salvus which translates to safe referring to its medicinal properties. In the Americas, Salvia is known not only for its medicinal but also for spiritual properties. For instance, Salvia divinorum (also known as sage of the seers) is popular for its use in shamanism by the Mazatecs. Traditionally it is used during spiritual healing sessions, when the shamans need to go deep in the supernatural world to discern the cause of the patient’s state. After consuming the herb, the shaman travels in visionary states of consciousness that will concede the steps to cure the patient. Believe it or not, it definitely sounds like a fascinating experience. But as a flower morphologist, there are some other particularities that I would also classify as fascinatingly interesting. And yes, I am obviously talking about floral structures, one in particular that has changed the whole evolutionary path of Salvia.

Traditional Mazatec Shaman ceremony with Salvia divinorum
Source: https://www.vice.com/en_us/article/salvia-velada-mazatec-shaman-ceremony-portfolio-v23n8

Salvia is a widely distributed genus of nearly 1000 species, all of which share a unique pollination strategy known as the staminal lever mechanism. Like almost any member of Lamiales, the number of stamens varies from two to five in different species. In fact, there is a tendency in this group for a reduction or complete absence of the posterior stamens (i.e., stamens at the top) as a consequence of bilateral symmetry (learn more here). However this doesn’t seem to affect pollination efficiency, and there are many examples of pollination strategies where flowers tend to package their pollen or develop complex structures to restrict pollen collection in a single flower visit.

Flower diversity in Salvia 

Sources: Flickr (1, 3, 4, 5), Flora-on (2), Flowers in Israel (6)

In Salvia, flowers have only two stamens, and the stamen’s connective which separates the thecae of each anther becomes elongated. This elongation of the stamen connective varies in length from species to species, and it is this abnormal length of the stamen connective that allows the formation of a lever mechanism. And this lever mechanism is considered to be a key innovation since it created a very effective pollination artifice for which Salvia is best known.

But how exactly does this mechanism work? 

What happened in the course of evolution of the Salvia androecium is that the posterior thecae of each stamen became unfertile and both fused together, creating a structure called the lower lever arm. This structure is centrally located on the base of the corolla’s entrance, whereas the fertile thecae stay on the upper lip of the corolla. When a nectar seeking pollinator enters the flower, it compresses the lower lever arm, and the fertile thecae immediately deposit the pollen on the back of the pollinator.

Evolution of the staminal lever in Salvia

1 – Ancestral state of androecium morphology in Salvia (generalized trend within tribe Mentheae); 2 – Funcional loss of the posterior stamens; 3 and 4 – Elongation of connective tissue between both thecae; 5 – functional abortion and fusion of both posterior thecae, the lower lever arm is formed!; Picture: Walker & Sytsma 2006 

The pollen deposition systems are highly precise in Salvia species with a high level of specialization to different pollinators, and even to different parts of the body of the same species of bee (learn more here). This has driven the evolution and radiation of the entire genus. This radiation is the reason why the lever mechanism is considered to be a key innovation – because it lead to a boom of diversification.

Examples of pollen deposition systems in Salvia

A: Pollen transfer in Salvia pratensis; top picture is a scheme of the mechanism of the lever; bottom left picture shows a pollinator entering a young flower to access the nectar, pushing the lever (in black) and triggering pollen loading on its back; bottom right picture show a later stage of the same flower, in which the style (in black) takes the position of the stamens (not represented here) and the insect deposits the pollen collected in another flower of the same species on the stigma of this one; Picture: Claßen-Bockhoffet al 2004; B: Pollen transfer in Salvia lanceolata – to access the nectary (n), the pollinator (Nectarinia chalybea) pushes the lever arms (pc) and the thecae (t) at the anterior connective arms (ac) move down to deposit the pollen on the bird’s head, j is the joint between filament and connective that enable this movement; Picture: Wester & Claßen-Bockhoff 2007

Of course, as all Salvia’s share this unusual pollination syndrome that relies on such a complex staminal structure, botanists used to believe that Salvia only speciated after the evolution of the staminal lever. That Salvia was monophyletic (i.e. shared a common ancestor) and the staminal lever evolved only once. But it’s a trap! Recent studies have actually revealed that Salvia is actually polyphyletic (i.e., the lever arm evolved many times). Thus, what we classified as a single genus in the past is actually four distinct evolutionary lineages that have evolved in parallel (learn more here). Though I still find it hard to believe such structure evolved so many times, this proves we botanists, have alot to learn about plant evolution. But isn’t it wonderful to know there is still so much to learn?!

Cyathium, the astounding performer

“What is the cyathium, this astounding performer?” wondered León Croizat in his “On the classification of Euphorbia” (1937).

The (literally) most beautiful Euphorbia, E. pulcherrima (from the latin pulcher / pulcherra = beautiful; pulcherrimum / pulcherrima = the most beautiful), stars in this festive season. It seems to be therefore an appropriate occasion to unfold the Euphorbia topic.

The story of E. pulcherrima begins from a very far distance to Christianity or Christmas traditions. The plant is native to Mexico, and has been well known to the Aztecs who used it to make red dye and as a fever cure.

Wild Euphorbia pulcherrima in Mexico.
Picture: Mark E. Olson

It was only in 1825 that it was first brought to the US by the ambassador Joel Roberts Poinsett – hence their common name, Poinsettia. Its undeniable extravagance due to the vibrant contrast between the intense red bracts and the deep green leaves rapidly made E. pulcherrima a popular species in horticulture. Being a December bloom, it soon became a favourite in Christmas decorations, which very much increased its popularity.

Joel Roberts Poinsett

The structure of Euphorbia flowers is a trend topic in botany classes because of their striking strangeness. This striking strange appearance is assigned to their being strikingly simple and complex at the same time. Euphorbia flowers are actually too simple to be called complex for the complexity does not lie in the flower itself, but on the organization of flowers within the inflorescence. It is so exquisite and unique that they gained a name for themselves – cyathium.

The structure of Euphorbia cyathium
Source: Euphorbiaceae.org

The cyathium is derived from a cymose-type inflorescence, and consists of a terminal female flower surrounded by prophylls (bracteoles) subtending the male flowers and forming the involucrum. Each flower consists of a single organ, so female flowers consist of a single pistil with the very typical 3-locular ovary (three carpels) and bifid styles, and male flowers consist of a single stamen. As there are no petals or sepals associated to the flowers, the cyathium develops bracts (cyathophylls) and large nectar glands for pollination purposes.

Cyathium of Euphorbia pulcherrima. Picture: Marc Perkins

But the cyathium structure is itself diverse, after all Euphorbia is a huge genus with around 2500 described species scattered around the globe (!!) – no wonder diversity is enormous. Some species (e.g., E. milii) have single cyathia with their own cyathophylls (two per cyathium). Others (e.g., E. albomarginata) have glands with petaloid appendages, resembling the classic structure of angiosperm flowers. E. pulcherrima, on the other hand, forms synflorescences, which in botanical language simply means a group of inflorescences (botanists really fancy throwing complicated names just because). So, E. pulcherrima forms cyathia lacking cyathophylls, which are grouped in synflorescences; therefore the red bracts so characteristic of poinsettias are not cyathophylls. Some authors don’t even consider these as being bracts, but simply as leaves that turn color, so you may find them described as bracteate leaves…

Left picture: Euphorbia milii (Source: Subhin)
Right picture: Euphorbia albomarginata (Source: Jason Penney)

I could continue endlessly writing about Euphorbias, but before getting too extended on the subject, I shall stop this post at once to wish all readers a fantastic holiday and a 2016 blooming with happiness.

Picture: Pauline Brock

Putting all eggs in one basket

When competition is high, plants have to be creative to explore the diversity of the available potential pollinators. Not all pollinators are attracted to fruity, sweet scents and flavours; some flies, for example, feed and lay their eggs on flesh of rotting animals, thus the smell of fresh carcasses are a temptation for these flies! Flowers, pliant as they are, can imitate this smell, deceiving the hungry flying creatures to the illusive corpse feast. I could name a few species of plants with this kind of strategy, but for now I will focus on one species – the titan arum, a plant from Sumatra (Indonesia) famous for being ridiculous on both size and smell – the kind of eccentricity that like to grow in tropical rainforests.

Two titan arums in Sumatra, early 1900's. The inflorescence (right) can reach over 3 metres in height, whereas the leaf (left) can reach up to 6 metres tall!

 Titan arum, Amorphophallus titanum (Araceae) does have the largest inflorescence described so far. Yes, that is not a flower, but a pseudanthium. A pseudanthium is defined to be an inflorescence that mimics a flower, thus the flowers are usually very small and strategically packed in compact inflorescences. In Araceae, the structure that bears the flowers is called a spadix, which is generally enclosed in a big showy bract – the spathe. Interestingly, the visible part of the spadix is not fertile, and acts as an osmophore, essential for an effective pollination in this family of plants. It is here where this fetid (but magic) pollination story starts: the osmophores (floral fragrance glands) produce the smell, which will attract all sorts of flies and beetles. Of course the smell has to be really intense to reach vast distances in a tropical forest, so the spadix also produces a great deal of heat (up to 40ºC in A. titanum!), which is believed to help convey the scent further. Isn’t it fascinating?!

The inflorescence is formed by the spadix and a big bract called spathe.
Photo: David A. Purvis (New Reekie in bloom at the Royal Botanic Garden Edinburgh, June 2015)

The fertile parts of the spadix (the flowers) are hidden by the spathe in a space called floral chamber. Araceae are known for being really good hosts for theirs pollinators: once the visitors arrive, they sneak into the floral chamber where they can spend a peaceful night, protected from night dangers and feed their bellies with some pollen. Meanwhile, they hang around on flowers, obviously some of that pollen gets attached to their bodies and carried away to the next pseudanthium the following morning.

Entrance to the floral chamber: flowers are already visible at the base the of spadix
Photo: Chlorophil7

Araceae flowers are usually very small and reduced to the essential parts – the sexual organs. So the tepals are absent or highly reduced; male flowers are reduced to a single stamen, and female flowers to a single carpel.  Now, I haven’t been counting them, but it is said that in one single A. titanum pseudanthium the number of female flowers can go up to about 450, condensed in the base of the inflorescence. Male flowers (as are smaller) can be even more, ranging from 500 to 1000. To avoid self-pollination, female flowers are receptive earlier. So, when the male flowers start releasing fertile pollen, the stigmas of the same inflorescences are not receptive anymore, and there is no danger of self-pollination. It is also very common in Araceae the formation of infertile male flowers (also called staminodes, as each flower corresponds to one single stamen), the function of these staminodes is not very clear yet. Titan arum, however, seems to lack such staminodes.

The base of the spadix bears both male flowers (single-stamen flowers; top of the inflorescence) and female flowers (single-pistil flowers; base of the inflorescence).
Left photo: isenbergs2007; Right photo: Brian 

As you can imagine, producing such a big structure, plus all that smell and heat is a great expense of energy resources. Thus, the plant only flowers for about 3 days every thousand days (I have learned this one from Sir David Attenborough).

David Attenborough with a wild Amorphophallus titanum in Sumatra filming for BBC's The Private Life of Plants

Titan arum is quite a fantastic plant, not only it looks unreal but it is incredible how such a rare flowering event is enough to succeed on fruit production and perpetuate the lineage… It seems to be the case where "putting all eggs in one basket" actually works.

Feminine sophistication

Gynoecium is without a doubt the most complex organ in a flower. It is here where all the magic of fertilization happens, where pollen meets the ovule and embryos are formed. It has the responsibility of protecting, nurturing and, ultimately, spreading the seeds, not as gynoecium anymore, but as the fruit – the result of its the development. Of course a structure where most action (and purpose) in a plant’s life takes place must be of great sophistication.

Some species, not happy with having solely an ovary, decided to create a peculiar one. In Punica granatum (Lythraceae), the pomegranate – the gynoecium is a highly complex organ and it’s hard to compete with such unique structure.

Pomegranate flower (right) and developing fruit (left).
Foto: Reji

Carpels are placed in different whorls (usually 2 to 3 whorls of carpels), which culminate on a great mess of carpels, arranged in superposed layers in one single ovary (please, take a look at the image!).

Scheme of pomegranate ovary showing layered whorls of carpels. (Original picture: Sinha & Joshi, 1959)

Generally (syncarpous) ovaries are placed in one single whorl due to space constraints. A multi-whorled ovary implies a great deal of logistics, and I wonder what happened in the course of evolution to have such a complex structure selected, a rarity among angiosperms.

But Punica granatum is also unique with respect to the placentation of the ovules. If you observe the ovary, you can see that basal carpels tend to have axile placentation, whereas upper carpels seem to have parietal placentation. Such differences are related with the development of the ovary, but before despair, take a look at the picture below and allow me to explain what is going on in this ovary.

Schematic representation of the growth of carpels. Placentation is axile in all whorls but in the uppermost whorl the placenta is always on the peripheral side of the locule because of the carpels growth. (Original picture: Sinha & Joshi, 1959)

What happens in P. granatum is that placentation is always axile, including the upper whorl. However, because carpels are on the inner surface of a deep floral cup, the inclination of the carpels of the upper (outer) whorl is different from that in the lower (inner) whorl. Thus, the carpels of the upper whorl are directed obliquely downwards, giving the wrong impression of having a parietal placenta. That they are not parietal can already be seen in the fact that they have septa, as gynoecia with parietal placentation have no septa.

Axile vs. parietal placentation

Now, before finishing this post, allow me to clarify the structure of Punica’s fruit. The mesocarp (the fleshy tissue that we eat in many fruits, such as apples, pears, plums, apricots, etc) is represented in pomegranates as a thin white layer – the tissue wall that separates the carpels ovaries. The fleshy part of this fruit is unusually the testa of seeds (or seed coat), and it is called a sarcotesta – the botanical name for fleshy testa. The sarcotesta is many times described as an aril, but it has nothing to do with the aril found in Taxus fruits, which is an appendage of the fruit – different from the outermost layer of the seed. 

The edible part of most fruits is the ovary's mesocarp; in Punica granatum we eat seeds' sarcotesta instead.
(Foto: Eric Beaume)

The symbolism of the pomegranate is present in many cultures from Western Asia to the Mediterranean basin. They tend to represent fertility and prosperity, which is not surprising regarding the numerous seeds each fruit bears and the incredible complexity around an already complex organ - the ovary.

Eucalypt flowers and the land of wildfires

One of the best things about my job is going to the field and last week this was made possible, my mission was to visit a eucalypt orchard and collect capsules of Eucalyptus globulus. Perfect! Since I had to collect capsules from the canopy, and eucalypt trees are quite tall, the orchard manager and me had to go in a crane to reach the top of the trees, I couldn’t believe it! It was fantastic and it truly made my day. Even though I have been in even taller canopies before, of different species, in different places and situations, it was for me as marvelous as the first time. It is always fascinating to reach a tree perspective from its canopy – sorry for not having pictures of the moment, but I had to share this with you anyway.

As I was there for capsule collection, I obviously took the chance of collecting some flowers too. I have been looking for eucalypt flowers for quite a while, but the canopies are tall, so I never managed to reach them (I don’t always find a crane next to the trees for a little canopy ride). Eucalypt flowers might not be extremely spectacular in terms of pollination, but their morphology is very interesting – and you have to agree it’s hard to stop looking at these beauties.

Eucalypt flowers diversity: 1 – Eucalyptus rhodantha; 2 – E. kingsmillii; 3 – E. synandra. 
(Photos: https://www.flickr.com/photos/tgerus/)

Since eucalypts belong to Myrtaceae, you do not expect a perianth here, stamens perform the attractive parts of the flower, and the colour attributed to the flower is actually the color of the stamens’ filaments. But even if you are not expecting to find a perianth, it doesn’t mean they don’t have one, or had… Eucalyptus’ perianth is replaced by a protective woody structure – the operculum, which falls at anthesis.

The operculum is maybe the most emblematic structure of the flowers of this genus, but it is not a new structure, it is a modified one instead. The origin of the operculum is actually on the fusion of perianth members (calyx and corolla), but in most groups (e.g. Symphyomyrtus subgenus) you will find two opercula in one flower bud: an outer operculum (of sepal origin) and an inner operculum (of petal origin). In these species, the sepal-derived operculum falls during bud development and the petal-derived one falls at anthesis. So, perianth exists, but is only there on early stages, before anthesis, leaving only a scar on the flower as a reminder of their existence.  

E. globulus flowers; The presence of a scar in the flower bud is a clear evidence that the outer operculum has fallen. Species with a single operculum, or fused opercula, lack this scar. (Photo: Bill Higham)

Another character of Myrtaceae, which has been discussed in another post is the hypanthium. The hypanthium is present in a number of groups, its morphology is labile, as well as the tissues involved, so do not expect to find identical hypanthia in different groups. Eucalypt hypanthia embed the inferior ovaries, and only the style is visible, between the stamina ring and base of the style.

E. globulus buds and flowers at early and later stages.
(Photos: Forest and Kim Starr)

In a later stage, this receptacular structure is involved in the formation of the capsule. Since hypanthium and ovary are structures intimately linked, maturation of the ovary takes place inside the hypanthium and a woody dehiscence capsule is formed. This is why eucalypt capsules are known to be false fruits, because the hypanthium is involved in the process and in the fruit structure. Finally, dehiscence takes place after capsules dry out (usually as a response to dead tissues caused by fire), and capsule opens through valves formed by the splitting of the ovary roof, corresponding to the locules.

When capsules dry out, the ovary roof splits in several valves and seeds are shed through these valves. The number of valves correspond to the number of ovary locules. Scars and rings, corresponding to floral organs, are also still visible in mature capsules. (Photo: John Tann)

Considering the dehiscence behavior and the ecology of eucalypts, I wonder if the formation of these false fruits are actually adaptations to fire. It has been already showed that eucalypt seeds are not fire-resistant, so seed viability relies on the insulating properties of the woody capsules. Perhaps two layers of tissue, the hypanthium combined with the ovary wall, provide higher insulating capacity?