Resin Midges, Basal Angiosperms, and a Strange Pollination Syndrome

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When we try to talk about clades that are "basal" or "sister" to large taxonomic groups, your average listener either consciously or unconsciously thinks "primitive." Primitive has connotations of something that under-developed or unfinished. This is simply not the case. Take, for instance, a family of basal angiosperms called Schisandraceae.

This family is nestled within the order Austrobaileyales, which, along with a small handful of other families, represent the earliest branches of the angiosperm family tree still alive today.  To call them primitive, however, would be a serious misnomer. Because they diverged so early on, these lineages represent serious success stories in flowering plant evolution, having survived for hundreds of millions of years. Instead, we must think of them as fruitful early experiments in angiosperm evolution.

Floral morphology of and interaction between midge and their larvae (white arrows) in Illicium dunnianum

Still, the proverbial proof is in the pudding and if there was any sort of physical evidence one could put forth to remove our hierarchical prejudices about the taxonomic position of these plants, it would have to be their bizarrely specific pollination syndromes.  Members of the family Schisandraceae have entered into intense relationships with a group of flies known as midges and their interactions are anything but primitive. 

We will start with two species of plant native throughout parts of Asia. Meet as Illicium dunnianum and Illicium tsangii. More will be familiar with this genus than they may realize as Illicium gives us the dreaded star anise flavor our grandparents liked to sneak into our cookies as kids (but I digress). These particular species, however, have more to offer the world than flavoring. They are also very important plants for a group of gall midges in the genus Clinodiplosis.

The midges cannot reproduce without I. dunnianum or I. tsangii. You see, these midges lay their eggs within the flowers of these plants and, in doing so, end up pollinating them in the process. At first glance it may seem like a very one-sided relationship. Female midges deposit their eggs all along the carpels packed away inside large, fleshy whorl of tepals. As the midges crawl all over the reproductive organs looking for a suitable place to lay, they inevitably pick up and deposit pollen. 

Floral morphology and interaction between midge larvae (white arrows) in  Illicium tsangii

This is not the end of this relationship though. After eggs have been deposited, something strange happens to the Illicium flowers. For starters, they develop nursery chambers around the midge larvae. Additionally, their tepals begin producing heat. Enough heat is produced to keep the nursery chamber temperature significantly warmer than the ambient air temperature. What's more flower heating intensifies throughout the duration of fruit development. It was originally hypothesized that this heating had something to do with floral odor volatilization and seed incubation, however, experiments have shown that at least seed development in these two shrubs is not influenced by floral heat in any major way. The same cannot be said for the midge larvae. 

As the flowers mature and give way to developing seeds, the midge larvae are hard at work feeding on tiny bits of the flowers themselves. When researchers looked at midge larvae development on these Illicium species, they found that they were completely dependent upon the floral heat for survival. Any significant drop in temperature caused them to die. Essentially, the plants appear to be producing heat more for the midges than for themselves. It may seem odd that these two plants would invest so much energy to heat their flowers so that midge larvae feeding on their tissues can survive but such face-value opinions rarely stand in ecology.

One must not forget that those larvae grow up to be adult midges that will go on to pollinate the Illicium flowers the following season. Although the plants are taking a bit of a hit by allowing the larvae to develop within their tissues, they are nonetheless ensuring that enough pollinators will be around to repeat the process again. If that wasn't cool enough, the relationship between each of these plants and their pollinators are rather specific and the authors of at least one paper believe that the midges that pollinate each species are new to science. 

Now, if I haven't managed to convince you that this angiosperm sister lineage is anything but primitive, then let's take a look at another genus within the family Schisandraceae that have taken this midge pollination syndrome to the next level. This story also takes place in Asia but instead involves a genus of woody vines known as Kadsura

Like the Illicium we mentioned earlier, a handful of Kadsura species rely on midges for pollination. The way in which they go about maintaining this relationship is a bit more involved. The midges that are attracted by Kadsura flowers are known as resin midges and their larvae live off of plant resins. The flowers of Kadsura are another story entirely. They are as odd as they are beautiful. 

Flowers, pollinators ,and their larvae (white arrows) in  Kadsura heteroclita .

Flowers, pollinators ,and their larvae (white arrows) in Kadsura heteroclita.

In male flowers, stamens are arranged in dense, cone-like structures called androecia whereas the female flowers contain a compact shield-like structure with the uppermost part of the stigma barely emerging. This is called a gynoecium. Even weirder, the male flowers of one particularly strange species, Kadsura coccinea, produce large, swollen inner tepals. 

Once Kadsura flowers begin to open, visiting midges are not far behind. Male flowers seem to attract more midges than female flowers and it is thought that this has to do with varying amounts of special attractant chemicals produced by the flowers themselves. Regardless, midges set to work exploring the blooms with males looking for mates and females looking for a place to lay their eggs. 

When a suitable spot has been found, females will deposit their eggs into the floral tissues with their ovipositor. The wounded plant tissues immediately begin producing resin, not unlike a wounded pine tree. In the case of K. coccinea, it would appear that the oddly swollen tepals are specifically targeted by female midges for egg laying. They too produce resin upon having eggs laid within. 

The oddball flowers of Kadsura coccinea showing swollen tepals.

The function of plant resins in many cases are to fight off pathogens. From beetles to fungi, resin helps plug up and seal off wounds. This does not seem to be the case in the Kadsura-midge relationship though. The so-called "brood chambers" within the floral tissues go on producing resin for upwards of 6 days after the midge eggs were laid. Eventually the floral parts whither and drop off but the midge larvae seem to be quite happy in their resin-filled homes. 

As it turns out, the resin midge larvae feed on the viscous resin as their sole food source. Instead of trying to ward off these pesky little insects, the plants seem to be encouraging them to raise their offspring within! Just as we saw in the Asian Illicium, these Kadsura vines seem to be providing brood sites for their pollinators. Also, just as the Illicium-midge relationship thought to be species specific, each species of Kadsura appears to have its own specific species of resin midge pollinator! K. coccinea even goes as far as to produce tepals specifically geared towards raising midge larvae, thus keeping them away from their more valuable reproductive organs. In return for the nursery service, Kadsura have their pollinators all to themselves.

Pollination mutualisms in which plants trade raising larvae for pollen transfer are extremely derived and some of the most specialize plant/animal interactions on the planet. To find such relationships in these basal or sister lineages is living proof that these plants are anything but primitive. In the energy-reproductive investment trade-off, it appears that ensuring ample pollinator opportunities far outweighs the cost of providing them with nursery chambers. It is remarkable to think just how intertwined the relationships between these plants and there pollinators truly are. Take that, plant taxonomic prejudices! 

Photo Credits: [1] [2]

Further Reading: [1] [2] 

 

Devil's Gardens

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Imagine, if you will, walking through the dense understory somewhere in the Amazon basin. Diversity reigns supreme here and it would seem that every few steps reveals myriad new plant species. As you walk along, something in the vegetation changes. You stumble into a clearing in the middle of the forest dominated entirely by a single species of tree. Why the sudden change? How did this monoculture develop? You, my friend, have just found yourself on the edge of a Devil's garden. 

Devil's gardens are said to be the resting place of an evil spirit known to local tribes as Chullachaki. Anyone unlucky enough to stumble into his garden is said at risk of attack or curse. In reality, these gardens have a biological origin. The real gardeners are a handful of ant species which seem to have rather specific gardening preferences. Careful inspection would reveal that the gardens largely consist of trees in one of three genera - Duroia, Tococa, or Clidemia

Tococa  sp. (Melastomataceae)

Tococa sp. (Melastomataceae)

The reason that ants are so fond of these genera has to do with housing. These plant groups contain species which produce swellings along their stems and petioles known as domatia. These domatia are hollow and are the favorite nesting spots of various ant species. Ant colonies set up shop within. As anyone who has ever blundered into an ant colony can attest, ants are quite voracious at defending their home. 

By providing ant colonies with a home base, these plants have essentially hired body guards. It is a wonderful form of symbiosis in which the ants aggressively defend against anything that might want to take a bite out of their host tree. Any herbivore trying to take up residence or lay eggs within the Devil's garden is viciously attacked. In doing so, the ants are protecting their host trees at the cost of all other plants unlucky enough to germinate within the garden. Still, this anti-herbivore behavior doesn't totally explain the monoculture status these host trees achieve within the garden itself. Why are these gardens so ominously devoid of other plant species?

To answer this, one would have to watch how the ants behave as they forage. While scouting, if ants encounter a seedling of their host tree, nothing really happens. They go about their business and let the seedling grow into a future home. When they encounter a non-host tree, however, their behavior completely changes. 

Behold - A Devil's Garden

Behold - A Devil's Garden

The ants begin biting the stem of the plant, exposing its vascular tissue. As they bite, the ants also sting the foreign seedling, injecting minute amounts of formic acid into the wound. One or two ants isn't enough to bring down a seedling but one thing ants have on their side are numbers. Soon an entire platoon of ants descend upon the hapless seedling, stinging it repeatedly. In no time at all, the seedling succumbs to the formic acid injections and dies. By repeating this process any time a foreign plant is found growing within the vicinity of the garden, the resident ants ensure that only trees that will produce domatia are allowed to grow in their garden. Thus, a Devil's garden has been formed. 

Although this relationship seems incredibly beneficial for each party, it does come at some cost to the plants themselves. Certainly forming the domatia is a costly endeavor on the part of the plant, but research has also shown that growing in such high, monoculture-like densities in the jungle has its downsides. It has been found that individual host trees can actually experience more herbivore pressures when growing within a Devil's garden than if it was growing alone, elsewhere in the forest. 

Despite their aggression towards herbivores, the ants simply cannot be everywhere at once. As such, the high densities of host tree species within a Devil's garden act like a dinner bell for any insect that enjoys feeding on that particular type of plant. Essentially, the ants are concentrating a potential food source. Experts believe that this might explain why Devil's gardens never completely take over entire swaths of forest. Essentially, there are diminishing returns to living in such high densities. Still, benefits must outweigh costs if such mutualisms are to be maintained and it is quite obvious that both plant and ant benefit from this interaction to a great degree. 

Photo Credits: [1] [2] [3] [4]

Further Reading: [1] [2] [3] [4]

Bowerbirds - Accidental Gardeners

To look upon the bower of a male bowerbird is to see something bizarrely familiar. These are not elaborate nests but rather architectural monuments whose sole purpose is to serve as a staging ground for mating displays. Males build and adorn these structures with precision and a sense of aesthetics. Because of this behavior, at least one species of bowerbird, the spotted bowerbird, can add another occupation to its resume - accidental gardener.

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When a male finds a certain color he likes, he scours the landscape in search of these treasures. For many male bowerbirds, fruits offer a wide array of colors and textures of which they can add to their menagerie. Male spotted bowerbirds seem to have a fondness for the fruits of the potato bush (Solanum ellipticum). Their stark green hue contrasts nicely with the bower architecture.

When the fruits start to decompose, they no longer serve any purpose for the male bowerbird and he tosses them aside. Seeds begin to accumulate around the bower and after some time they will germinate. Researchers decided to investigate this relationship a bit further. What they found was pretty astounding.

They discovered that bush potato plants grew in higher numbers around bowers than they do at random locations throughout the forest. What's more, the fruits produced by bush potatoes growing near bowers were much greener than those of plants elsewhere. In effect, male spotted bowerbirds are not only cultivating the bush potato, they are also artificially selecting for improved coloration of its fruits.

To date, this is the only example of something other than a human cultivating a plant for reasons other than food. The similarities between human cultivation and bowerbird cultivation are mind blowing. Similar to human farmers, male bowerbirds clear the site of competing vegetation and remove the fuel load so as to minimize the risk of fire, all of which provides ideal habitat for germination. Though the male bowerbirds are not intentionally cultivating the bush potato, they have nonetheless entered into a mutualistic relationship in which the males get ready access to beautiful fruits and in return, the bush potato gets a nice, safe place to grow.

Photo Credit: University of Exeter and bit.ly/1T29wjN

Further Reading:

http://www.sciencedirect.com/science/article/pii/S0960982212002084