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?!

The majestic legends of a Sacred & Sad Tree

Had fell in love, couldn’t avoid the pain for this love wasn’t reciprocal, becoming sorrowful for the whole eternity.

In short, this is the legend I heard about a tree native to the Indian sub-continent – the Parijat or sad tree. The reason for such a name is something that always made me curious – why was this plant condemned to have such a dreadful and miserable destiny? Of course it had to have love involved at some level. After all, isn’t love the mother of all emotions? Love or the absence of love is the root of all feelings and such a pain that lasts the whole eternity had to be linked with this. 

Let’s start by dissecting the scientific name of the plant, Nyctanthes arbor-tristis means literally “night-blooming sad tree”, so it does give us already a clue about the behaviour of the plant – flowers bloom at night. Taking a look at the flower and blooming patterns, the candidate pollinator can be guessed. The flowers are definitely designed to attract night-pollinators – the colour, the night-blooming condition and the characteristic sweet fragrance that Oleaceae is well-known to exude is also very strong at night. Linked with the size and shape of the flowers, I can only think of a moth to do this kind of job!

One of the legends say that the heavenly Parijat tree was brought to this world by Lord Krishna as a gift for one of his wives, Rukmini. [Source: www.indianminiaturepaintings.co.uk]

As I mentioned in the beginning of this post, the first legend I heard is about an Indian princess, Parijat who fell in love with Surya-deva (the Sun-god), which deserted her. Heart-broken and in despair, the princess committed suicide, was cremated and brought back to life from the ashes in the form of a tree. Incapable to bear the sight of the one that lead her to kill herself, the flowers only bloom at night, and it is said that the flowers are shed like tear-drops in the first shade of dawn. It is a romantic but cruel story from which Linnaeus was probably based to name the tree. But apart from this one, there is a much important story that puts this plant into a sacred level in several Asian religions as Jainism, Hinduism and Buddhism. The Parijat tree is linked with a very famous episode from the sacred texts Puranas that describes a wish-fulfilling divine tree formed during the Churning of the Milky Ocean. Other legends were made around this incredible tree, but it would be an endless post if I start telling them all!

Sagar Manthan by Raja Ravi Varma representing the Churning of the Milky Ocean, and the Parijat tree represented as one of the treasures churned by the gods

No wonder though that this tree, known to be sorrowful, is full of stories and legends around it. It has a special behaviour, and descriptions say that the fragrance produced take us to drawn into its sweetness – it perfumes the entire universe it is said and so its essential oil is used in perfume-making. Also, it is popular for medicinal purposes in Asia, including Ayurvedic medicine.

The flower of Nyctanthes arbor-tristis. [Source: Saroj Kumar Kasaju]

Botanically it might be a bit boring – or is it?! This is Oleaceae, we are in the realm of Lamiales, the land of merism hodgepodge. But in Oleaceae things seem to be more pacific and there is a pattern we can rely on: usually flowers are hanged in the tips of branches forming wonderful cymoses of rather small flowers. These usually have four petals and two stamens, so it seems to be quite easy to spot a member of the Oleaceae family. But because this lovely one has to be special in every field, the merism is higher here than in the rest of the family (along with some Jasminum) and the number of petals can go from 5 to 8. 

I am only sorry that we cannot feel fragrances through internet yet! :)

A Mid-Night Horror Story

Imagine you’re walking around in the forest at night and suddenly you find a pile of thin bones, you look up and you see a tree with dangling sickles and bats flying over… Creepy, uh? Well, maybe if you look a little bit closer the bones are not real bones, they are fallen branches and there are no sickles, they are just the fruits of this bat-pollinated tree – but that was scary enough! Today’s story is about the “Midnight Horror”!

The midnight horror tree, Oroxylum indicum, is a very popular tree in Southeast Asia due to their weird appearance, but despite of this, there is no reason to fear it - in fact most of the plant is used for medicinal purposes (leaves, seeds, bark and roots).

Oroxylum indicum. On the left side: the tree with hanging fruits; on the right side: the flowers.

Oroxylum indicum belongs to the Bignoniaceae family, a family with tropical distribution, belonging to the problematic Lamiales order. Lamiales encomprises some closely related and big families such as Lamiaceae, Acanthaceae, Oleaceae, Gesneriaceae, Scrophulariaceae, Plantaginaceae, Verbenaceae… The relationships between these families are not well understood and in many cases the morphological characters are not strong enough to determine the families’ delimitation, especially floral morphology. The typical Lamiales flowers have a well developed and basally fused calyx, a monosymmetric bilabiate corolla (upper and lower lips) and a superior bicarpellate ovary.

*Wow, botanists’ sophisticated dialect alert!*

Ok, ok… It is easier if I show some pictures, but what I want to show you here are the fluctuations on the number of stamens.

Typical Lamiales flowers. On the left: Lamiaceae, upper lip formed by 2 fused petals and lower lip formed by 3 fused petals; Dashed line representing the monosymmetric corolla. On the right side: Orobanchaceae, upper and lower lips fused forming the corolla tube; the calyx is fused on the base. 

In Lamiales the androecium varies from one to five stamens, including reductions of stamens into staminodes (sterile stamens) which are not well understood. This character is highly variable, and in my opinion is due to the current evolution of the group. This means that the characters for families’ circumscription are not well established yet, giving this morphological fluctuation as a consequence.

However, Bignoniaceae, has some characters restricted to the family, which makes it easy to spot in the field. The flowers in this family are very big, colourful and showy – hard not to see. They usually also have big nectarines in the base of the flower, releasing a strong and sweet fragrance – no wonder they are pollinated by big animals such as bats! Usually they have 4 fertile stamens and 1 unfertile stamen (staminode), but this species in particular has 5 fertile stamens and no staminodes. I have also found Bignoniaceae flowers with more variation, but as I explained before, I believe the presence or absence of staminodes is possibly related with a transitional evolutionary state. The stigma (the female part which receives the pollen) is usually wet and relatively broad.

Typical Bignoniaceae flower with 2 pairs of stamens (long and short) and one staminode

 The essential vegetative character of the Lamiales is the simple-opposite leaves, but luckily Bignoniaceae has compound opposite leaves, and this makes our lives easier! Bignoniaceae are usually represented by trees, shrubs and are also well represented in tropical America by climbers, having the terminal leaflet differentiated into a tendril.

So don’t forget, whenever you see a tree or climber with big showy flowers with the petals fused into a tube, check for the leaves, if they are compound, you probably found a Bignoniaceae! In the case of the midnight horror tree, they have big white or whitish flowers, blooming and releasing a sweet scent at night – all perfect characters for efficient bat pollination.