Maxipiñon: One of the Rarest Pines in the World

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The maxipiñon (Pinus maximartinezii) is one of the rarest pines on Earth. A native of southern Sierra Madre Occidental, Mexico, nearly all individuals of this species can be found scattered over an area that collectively spans only about 3 to 6 square miles (5 – 10 km²) in size. Needless to say, the maxipiñon teeters on the brink of extinction. As a result, a lot of effort has been put forward to better understand this species and to develop plans aimed at ensuring it is not lost forever.

The maxipiñon has only been known to science for a few decades. It was described back in 1964 after botanist Jerzy Rzedowski noted some exceptionally large pine seeds for sale at a local market. He named the species in honor of Maximino Martínez, who contributed greatly to our understanding of Mexican conifers. However, it was very obvious that the maxipiñon was well known among the residents of Zacatecas.

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The reason for this are its seeds. The maxipiñon is said to produce the largest and most nutritious seeds of all the pines. As such, it is a staple of the regional diet. Conversations with local farmers suggest that it was much more common as recent as 60 years ago. Since then, its numbers have been greatly reduced. It soon became apparent that in order to save this species, we had to learn a lot more about what threatens its survival.

The most obvious place to start was recruitment. If any species is to survive, reproduction must outpace death. A survey of local markets revealed that a lot of maxipiñon seeds were being harvest from the wild. This would be fine if maxipiñon were widespread but this is not the case. Over-harvesting of seeds could spell disaster for a species with such small population sizes.

Indeed, surveys of wild maxipiñon revealed there to be only 2,000 to 2,500 mature individuals and almost no seedlings. However, mature trees do produce a considerable amount of cones. Therefore, the conclusion was made that seed harvesting may be the single largest threat to this tree. Subsequent research has suggested that seed harvests actually may not be the cause of its rarity. It turns out, maxipiñon population growth appears to be rather insensitive to the number of seeds produced each year. Instead, juvenile tree survival seems to form the biggest bottleneck to population growth.

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You see, this tree appears to be more limited by suitable germination sites than it does seed numbers. It doesn’t matter if thousands of seeds are produced if very few of them ever find a good spot to grow. Because of this, scientists feel that there are other more serious threats to the maxipiñon than seed harvesting. However, humans are still not off the hook. Other human activities proved to be far more damaging.

About 50 years ago, big changes were made to local farming practices. More and more land was being cleared for cattle grazing. Much of that clearing was done by purposefully setting fires. The bark of the maxipiñon is very thin, which makes it highly susceptible to fire. As fires burn through its habitat, many trees are killed. Those that survive must then contend with relentless overgrazing by cattle. If that wasn’t enough, the cleared land also becomes highly eroded, thus further reducing its suitability for maxipiñon regeneration. Taken together, these are the biggest threats to the ongoing survival of this pine. Its highly fragmented habitat no longer offers suitable sites for seedling growth and survival.

As with any species this rare, issues of genetic diversity also come into play. Though molecular analyses have shown that maxipiñon does not currently suffer from inbreeding, it has revealed some interesting data that give us hints into the deeper history of this species. Written in maxipiñon DNA is evidence of an extreme population bottleneck that occurred somewhere between 400 and 1000 years ago. It appears that this is not the first time this tree has undergone population decline.

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There are a few ways in which these data can be interpreted. One is that the maxipiñon evolved relatively recently from a small number of unique and isolated individuals. Perhaps a hybridization event occurred between two closely related piñon species - the weeping piñon (Pinus pinceana) and Nelson piñon (Pinus nelsonii). Another possibility, which does not rule out hybridization, is that the maxipiñon may actually be the result of artificial selection by agriculturists of the region. Considering the value of its seeds today, it is not hard to imagine farmers selecting and breeding piñon for larger seeds. It goes without saying that these claims are largely unsubstantiated and would require much more evidence to say with any certainty, however, there is plenty of evidence that civilizations like the Mayans were conserving and propagation useful tree species much earlier than this.

Despite all we have learned about the maxipiñon over the last few decades, the fate of this tree is far from secure. Ex situ conservation efforts are well underway and you can now see maxipiñon specimens growing in arboreta and botanical gardens around the world. Seeds from these populations are being used for storage and to propagate more trees. Sadly, until something is done to protect the habitat on which it relies, there is no telling how long this species will last in the wild. This is why habitat conservation efforts are so important. Please support local land conservation efforts in your area because the maxipiñon is but one species facing the loss of its habitat.

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

Further Reading [1] [2] [3]

The Largest Mistletoe

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When we think of mistletoes, we generally think about those epiphytic parasites living on branches way up in the canopy. The mistletoe we are discussing in this post, however, is a decent sized tree. Nuytsia floribunda is a native of western Australia where it is known locally as moojar or the Christmas tree. To the best of our knowledge, it is the largest mistletoe known to science.

Nuytsia floribunda is a member of the so-called showy mistletoe family (Loranthaceae). It along with all of its mistletoe cousins reside in the order Santalales but from a phylogenetic standpoint, the family Loranthaceae is considered sister to all other mistletoes. This has excited my botanists as it allows us a chance to better understand how parasitism may have evolved in this group as a whole.

Speaking of parasitism, there are some incredible things going on with N. floribunda that are worth talking about. For starters, it is not fully parasitic but rather hemiparasitic. As you can tell by looking at the tree decked out in a full canopy of leaves, N. floribunda is entirely capable of photosynthesizing on its own. In fact, experts feel that it is fully capable of meeting all of its own carbohydrate needs. Instead, it parasitizes other plants in order to acquire water and minerals. How it manages this is remarkable to say the least.

Nuytsia floribunda is a root parasite. Its own roots fan out into the surrounding soil looking for other roots to parasitize. Amazingly, exploratory roots of individual N. floribunda have been found upwards of 110 meters (360 ft.) or more away from the tree. When N. floribunda do find a suitable host root, something incredible happens. It begins to form specialized roots called “haustoria”, which to form a collar-like structure around the host’s roots.

Whole haustoria of Nuytsia (white [ha]) and host root (dark brown). * indicates `gland' and developing `cutting device.

Whole haustoria of Nuytsia (white [ha]) and host root (dark brown). * indicates `gland' and developing `cutting device.

The collar gradually swells and a small horn forms on the inside of the haustoria. Swelling of the haustoria is the result of an influx of water and as the pressure around the host root builds, the haustorial horn of N. floribunda physically cuts into its victim. Once this cut is formed, the haustoria form balloon-like outgrowths which intrude into the xylem tissues of the host root, thus forming the connection that allows N. floribunda to start stealing the water and minerals it needs.

Even more amazing is the fact that roots aren’t the only thing that N. floribunda will attempt to exploit. Many inanimate objects have been found wrapped up in a haustorial embrace including dead twigs, rocks, fertilizer granuals, and even electric cables! Its non-selective parasitic nature appears to have left it open to exploring other, albeit dead end options. I don’t want to paint the picture that this tree as the enemy of surrounding vegetation. It is worth noting that N. floribunda extracts very little from any given host so its impact is spread out among the surrounding vegetation, making its overall impact on host plants minimal most of the time.

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Provided its needs have been met, N. floribunda puts on one heck of a show around December. In fact, the timing of its blooms is the reason it earned the common name of Christmas tree. Flowering for this species is not a modest affair. Each tree is capable of producing multiple meter-long inflorescences decked out in sprays of bright orange to yellow flowers. The flowers themselves produce copious amounts of pollen and nectar, making it an important food source for resident pollinators. Though many different species have been documented visiting the flowers, it is thought that beetles and wasps are the most effective at pollination.

Seed dispersal for N. floribunda is mainly via wind. Each fruit is adorned with three prominent wings. After they detach from the tree, the fruits usually break apart into three samaras, each with its own wing. The key for success of any propagule is ending up in a site suitable for germination. According to some, this can be a bit tricky and attempts at cultivating this plant in captivity have not been terribly successful. It would seem that nature knows best when it comes to reproductive success in N. floribunda. It may be worth trying to figure it out though because recent evidence suggests that this species is not faring well with human development. As the surrounding landscapes of western Australia become more and more urbanized, plants like N. floribunda seem to be on the decline. Perhaps renewed interest in growing this species could change the tide for it as well as others.

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Photo Credits: [1] [2] [3] [4] [5]

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

The Creeping Strawberry Pine

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With its small, creeping habit and bright red, fleshy female cones, it is easy to see how Microcachrys tetragona earned its common name “creeping strawberry pine.” This miniature conifer is as adorable as it is interesting. With a fossil history that spans 66 million years of Earth’s history, it also has a lot to teach us about biogeography.

Today, the creeping strawberry pine can only be found growing naturally in western Tasmania. It is an alpine species, growing best in what is commonly referred to as alpine dwarf scrubland, above 1000 m (3280 ft) in elevation. Like the rest of the plants in such habitats, the creeping strawberry pine does not grow very tall at all. Instead, it creeps along the ground with its prostrate branches that barely extend more than 30 cm (0.9 ft) above the soil. This, of course, is likely an adaptation to its alpine environment. Plants that grow too tall frequently get knocked back by brutal winds and freezing temperatures among other things.

The typical growth habit of the creeping strawberry pine.

The typical growth habit of the creeping strawberry pine.

The creeping strawberry pine is not a member of the pine family (Pinaceae) but rather the podocarp family (Podocarpaceae). This family is interesting for a lot of reasons but one of the coolest is the fact that they are charismatic representatives of the so-called Antarctic flora. Along with a handful of other plant lineages, it is thought that Podocarpaceae arose during a time when most of the southern continents were combined into a supercontinent called Gondwana. Subsequent tectonic drift has seen the surviving members of this flora largely divided among the continents of the Southern Hemisphere. By combining current day distributions with fossil evidence, researchers are able to use families such as Podocarpaceae to tell a clearer picture of the history of life on Earth.

What is remarkable is that among the various podocarps, the genus Microcachrys produces pollen with a unique morphology. When researchers look at pollen under the microscope, whether extant or fossilized, they can say with certainty if it belongs to a Microcachrys or not. The picture we get from fossil evidence paints an interesting picture for Microcachrys diversity compared to what we see today. It turns out, Microcachrys endemic status is a more recent occurrence.

This distinctive, small, trisaccate pollen grain is typical of what you find with  Microcachrys  whereas all other podocarps produce bisaccate pollen.

This distinctive, small, trisaccate pollen grain is typical of what you find with Microcachrys whereas all other podocarps produce bisaccate pollen.

The creeping strawberry pine is what we call a peloendemic, meaning it belongs to a lineage that was once far more widespread but today exists in a relatively small geographic location. Fossilized pollen from Microcachrys has been found across the Southern Hemisphere, from South America, India, southern Africa, and even Antarctica. It would appear that as the continents continued to separate and environmental conditions changed, the mountains of Tasmania offered a final refuge for the sole remaining species in this lineage.

Another reason this tiny conifer is so charming are its fruit-like female cones. As they mature, the scales around the cone swell and become fleshy. Over time, they start to resemble a strawberry more than anything a gymnosperm would produce. This is yet another case of convergent evolution on a seed dispersal mechanism among a gymnosperm lineage. Birds are thought to be the main seed dispersers of the creeping strawberry pine and those bright red cones certainly have what it takes to catch the eye of a hungry bird. It must be working well for it too. Despite how narrow its range is from a global perspective, the creeping strawberry pine is said to be locally abundant and does not face the same conservation issues that many other members of its family currently face. Also, its unique appearance has made it something of a horticultural curiosity, especially among those who like to dabble in rock gardening.

Mature female cones look more like angiosperm fruit than a conifer cone.

Mature female cones look more like angiosperm fruit than a conifer cone.

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

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

Meet the She-Oaks

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No, what you are looking at here is not a type of conifer. Nor is it an oak. This odd plant belongs in its own family - Casuarinaceae. Despite their gymnosperm appearance, this is in fact a family of flowering plants. Though the name “she-oak” does hint at their larger position within the order Fagales, it was actually given to these trees in reference to the density of their wood in comparison to more commonly harvested oak species. Other common names for trees in this group include ironwood, bull-oak, beefwood.

As a whole this family sorts out as sister to Myricaceae in the order Fagales. It' is comprised of 4 genera (Allocasuarina, Casuarina, Ceuthostoma, and Gymnostoma) and roughly 91 species spread among Australia, Malaysia, and much of Polynesia. It is extremely difficult to make generalizations across so many species but there is one aspect of this family that makes them stand out - their appearance.

Gymnostoma  sp.

Gymnostoma sp.

Gymnostoma nobile  in Sarawak, Malaysia.

Gymnostoma nobile in Sarawak, Malaysia.

Without close inspection, one could be forgiven for thinking the various Casuarinaceae were species of conifer. For starters, their leaves have been reduced to tiny whorls surrounding their photosynthetic stems. The stems themselves have taken up the role of photosynthetic organs, which is one of the reasons this family is known for its drought tolerance. Reducing the surface area available for gas exchange helps to reduce water loss in the process. The stems themselves are arranged with whorls around the branches, giving them a rather bunched appearance. The photosynthetic branches are sometimes referred to as being ‘equisetiform’ as they superficially resemble the stems of Equisetum. They do not shed their photosynthetic branches and are therefore evergreen.

As mentioned, these are flowering plants. Their flowers themselves are aggregated into spike-like inflorescences near the tips of branches. Clusters of male flowers resemble catkin-like strobili and are often brightly colored. Female flowers are clustered into a more ovoid shape, with long, filamentous pistils sticking out like fiery, red pompoms. After fertilization, bracts at the base of the female flowers swell and the whole inflorescence starts to look more like some sort of a conifer cone than anything floral. This may have to do with the fact that, like conifers, the various Casuarinaceae are wind pollinated. Therefore, their reproductive structures have had to deal with similar selective forces related to optimizing pollen dispersal and capture.

Casuarina equisetifolia  with catkin-like male flowers and smaller, red female flowers.

Casuarina equisetifolia with catkin-like male flowers and smaller, red female flowers.

Allocasuarina distyla  female flowers and infructescence.

Allocasuarina distyla female flowers and infructescence.

Another interesting trait common to Casuarinaceae is the ability to fix nitrogen. The plants themselves don’t do the fixing, rather they form specialized nodules on their roots that house nitrogen-fixing bacteria. Unlike perennial legumes that regrow their nodules year after year, the members of Casuarinaceae hold onto their nodules, which can grow into impressive structures over time. This ability to house nitrogen-fixing bacteria is also shared with other members of the order Fagales, including members of Betulaceae and Myricaceae.

Thanks to the fact that they can tolerate drought, fix nitrogen, and have high timber value, species of Casuarinaceae have been introduced far outside of their native ranges. This has created yet another invasive species issue. Various Casuarinaceae have become serious pests in places like Central and South America, the Carribbean, and the Middle East. Control of such hardy plants can be extremely difficult once they reach a critical mass that maintains them on the landscape. Keep you eye out for these species. Not only are they interesting in their own right, knowing them can help you better understand their role in ecosystems both native and not.

Allocasuarina decaisneana  (Desert Oaks), Central Australia

Allocasuarina decaisneana (Desert Oaks), Central Australia

Photo Credits: [1] [2] [3] [4] [5] [6]

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

Crab Spiders and Pitcher Plants: A Dynamic Duo

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Most pitcher plants in the genus Nepenthes seem pretty adept at catching prey. These plants specialize in nutrient-poor soils and their carnivorous habit evolved as a means of supplementing their nutritional needs. Despite the highly evolved nature of their pitfall traps (which are actually modified leaves), Nepenthes aren’t perfect killing machines. In fact, some get a helping hand from seemingly unlikely partners.

Spend enough time reading about Nepenthes in the wild and you will see countless mentions of arthropods hanging around their pitchers. Some of these inevitably become prey, however, there are others that appear to be taking advantage of the plant. Nepenthes don’t passively trap arthropods. Instead, they lure them in with bright colors and the promise of tasty treats like nectar. This is not lost on predators like spiders, who are frequent denizens of pitcher mouths.

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Most notable to Nepenthes specialists are some of the crab spiders that frequently haunt Nepenthes traps. These wonderful arachnids sit at the mouth of the pitcher and ambush any insects that try to pay it a visit. Often times both predator and prey fall down into the pitcher, however, thanks to a strand of silk, the spiders easily climb back out with their meal. This may seem like bad news for the pitcher, however, recent research based out of the National University of Singapore has shown that this relationship is not entirely one sided.

By studying the interactions between spiders and pitcher plants both in the lab and in the field, ecologists discovered that at least one species of pitcher plant (Nepenthes gracilis) appears to benefit greatly from the presence of crab spiders. The key to understanding this relationship lies in the types of prey N. gracilis is able to capture when crab spiders are and are not present.

Not only did the presence of a resident crab spider increase the amount of prey in each Nepenthes pitcher, it also changed the types of insects that were being captured. Crab spiders are ambush predators that frequently attack prey much larger than themselves. It may seem as if this is a form of food robbery on the part of the crab spider but the spiders can’t eat everything. When they have eaten their fill, the spiders discard the carcass into the pitcher where the plant can make quick work digesting it for its own benefit.

Over time, simply having a spider hunting on the trap led to a marked increase in the number of insects in each pitcher compared to those without a spider. Even if these meals are already half eaten, the plant still gains nutrients. Additionally, the types of prey captured by pitchers with and without crab spiders changed. The spiders were able to capture and subdue insects like flesh flies, which normally aren’t captured by Nepenthes pitchers. As such, the resident crab spiders make available a larger suite of potential prey than would be available if they weren’t using the pitchers as hunting grounds.

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The crab spiders may benefit the pitcher plant in other ways as well. Research on crab spiders has shown that their bodies are covered in pigments that register high in the UV spectrum. Insects can see UV light and often use it as a means of finding flowers as plants often produce UV-specific pigments in their floral tissues. The wide array of UV patterns on flowers are there to guide their pollinators into position. Researchers have documented that insects are actually more likely to visit flowers with crab spiders than those without, which has led to the idea that UV pigments in crab spiders actually act as insect attractants. Visiting insects simply cannot resist the UV stimulus and quickly fall victim to the resident crab spider.

Could it be that by taking up residence on a Nepenthes pitcher, the crab spiders are increasing the likelihood of insects visiting the traps? This remains to be seen as such questions did not fall under the scope of this investigation. That being said, it certainly offers tantalizing evidence that there is more to the Nepenthes-crab spider relationship. More work is needed to say for sure but the closer we look at such interactions, the more spectacular they become!

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

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

The Japanese Umbrella Pine

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My first impression of the Japanese umbrella pine was that I was looking at a species of yew (Taxus spp.). Sure, its features were a bit more exaggerated than I was used to but what do I know? Trying to understand tree diversity is a recent development in my botanical obsession so I don’t have much to base my opinions on. Regardless, I am glad I gave the little sapling I was looking at a closer inspection. Turns out, the Japanese umbrella pine is most definitely not a yew. It is actually unique in its taxonomic position as the only member of the family Sciadopityaceae.

The Japanese umbrella pine goes by the scientific name of Sciadopitys verticillata. Both common and scientific names hint at the whorled arrangements of its “leaves.” I place leaves in quotes because they are not leaves at all. One of the most remarkable features of this tree is the fact that those whorled leaves are actually thickened, photosynthetic extensions of the stem known as “cladodes.”

Those tiny bumps along the stems are actually highly reduced leaves whereas the whorls of photosynthetic “leaves” are actually modified extensions of the stem called “cladodes.”

Those tiny bumps along the stems are actually highly reduced leaves whereas the whorls of photosynthetic “leaves” are actually modified extensions of the stem called “cladodes.”

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It seems that the true leaves of the Japanese umbrella pine have, through evolutionary time, been reduced to tiny, brown scales that clasp the stems. I am not sure what evolutionary advantage(s) cladodes infer over leaves, however, at least one source suggested that cladodes may have fewer stomata and therefore can help to reduce water loss. Until someone looks deeper into this mystery, we cannot say for sure.

As a tree, the Japanese umbrella pine is slow growing. Records show that young trees can take upwards of a decade to reach average human height. However, given time, the Japanese umbrella pine can grow into an impressive specimen. In the forests of Japan, it is possible to come across trees that are 65 to 100 ft (20 – 35 m) tall. It was once wide spread throughout much of southern Japan, however, an ever-increasing human population has seen that range reduced.

A 49.5 million years old fossil of a  Sciadopitys  cladode.

A 49.5 million years old fossil of a Sciadopitys cladode.

The gradual reduction of this species is not solely the fault of humans. Fossil evidence shows that the genus Sciadopitys was once wide spread throughout parts of Europe and Asia as well. Whereas the current diversity of this genus is limited to a single species, fossils of at least three extinct species have been found in rocks dating back to the Triassic Period, some 230 million years ago. It would appear that this obscure conifer family, like so many other gymnosperm lineages, has been on the decline for quite some time.

Despite the obscure strangeness of the Japanese umbrella tree, it has gained considerable popularity as a unique landscape tree. Because it hails from a relatively cool regions of Japan, the Japanese umbrella tree adapts quite well to temperate climates around the globe. Enough people have grown this tree that some cultivars even exist. Whether you see it as a specimen in an arboretum or growing in the wild, know that you are looking at something quite special. The Japanese umbrella tree is a throwback to the days when gymnosperms were the dominant plants on the landscape and we are extremely lucky that it made it through to our time.

Photo Credits: [1] [2] [3] [4] [5]

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

Resurrecting Café Marron

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Back in 1980, a school teacher on the island of Rodrigues sent his students out to look for plants. One of the students brought back a cutting of a shrub that astounded the botanical community. Ramosmania rodriguesii, more commonly known as café marron, was up until that point only known from one botanical description dating back to the 1800's. The shrub, which is a member of the coffee family, was thought to have been extinct due to pressures brought about during the colonization of the island (goats, invasive species, etc.). What the boy brought back was indeed a specimen of café marron but the individual he found turned out to be the only remaining plant on the island.

News of the plant quickly spread. It started to attract a lot of attention, not all of which was good. There is a belief among the locals that the plant is an herbal remedy for hangovers and venereal disease (hence its common name translates to ‘brown coffee’) and because of that, poaching was rampant. Branches and leaves were being hauled off at a rate that was sure to kill this single individual. It was so bad that multiple layers of fencing had to be erected to keep people away. It was clear that more was needed to save this shrub from certain extinction.

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Cuttings were taken and sent to Kew. After some trial and tribulation, a few of the cuttings successfully rooted. The clones grew and flourished. They even flowered on a regular basis. For a moment it looked like this plant had a chance. Unfortunately, café marron did not seem to want to self-pollinate. It was looking like this species was going to remain a so-called “living dead” representative of a species no longer able to live in the wild. That is until Carlos Magdalena (the man who saved the rarest water lily from extinction) got his hands on the plants.

The key to saving café marron was to somehow bypass its anti-selfing mechanism. Because so little was known about its biology, there was a lot of mystery surrounding its breeding mechanism. Though plenty of flowers were produced, it would appear that the only thing working on the plant were its anthers. They could get viable pollen but none of the stigmas appeared to be receptive. Could it be that the last remaining individual (and all of its subsequent clones) were males?

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This is where a little creativity and a lot of experience paid off. During some experiments with the flowers, it was discovered that by amputating the top of the stigma and placing pollen directly onto the wound one could coax fertilization ans fruiting. From that initial fruit, seven seeds were produced. These seeds were quickly sent to the propagation lab but unfortunately the seedlings were never able to establish. Still, this was the first indication that there was some hope left for the café marron.

After subsequent attempts at the stigma amputation method ended in failure, it was decided that perhaps something about the growing conditions of the first plant were the missing piece of this puzzle. Indeed, by repeating the same conditions the first individual was exposed to, Carlos and his team were able to coax some changes out of the flowering efforts of some clones. Plants growing in warmer conditions started to produce flowers of a slightly different morphology towards the end of the blooming cycle. After nearly 300 attempts at pollinating these flowers, a handful of fruits were formed!

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From these fruits, over 100 viable seeds were produced. What’s more, these seeds germinated and the seedlings successfully established. Even more exciting, the seedlings were a healthy mix of both male and female plants. Carlos and his team learned a lot about the biology of this species in the process. Thanks to their dedicated work, we now know that café marron is protandrous meaning its male flowers are produced before female flowers.

However, the story doesn’t end here. Something surprising happened as the seedlings continued to grow. The resulting offspring looked nothing like the adult plant. Whereas the adult plant has round, green leaves, the juveniles were brownish and lance shaped. This was quite a puzzle but not entirely surprising because the immature stage of this shrub was not known to science. Amazingly, as the plants matured they eventually morphed into the adult form. It would appear that there is more to the mystery of this species than botanists ever realized. The question remained, why go through such drastically different life stages?

A young café marron showing its brown, mottled, lance-shaped leaves.

A young café marron showing its brown, mottled, lance-shaped leaves.

The answer has to do with café marron's natural predator, a species of giant tortoise. The tortoises are attracted to the bright green leaves of the adult plant. By growing dull, brown, skinny leaves while it is still at convenient grazing height, the plant makes itself almost invisible to the tortoise. It is not until the plant is out of the range of this armoured herbivore that it morphs into its adult form. Essentially the young plants camouflage themselves from the most prominent herbivore on the island.

Thanks to the efforts of Carlos and his team at Kew, over 1000 seeds have been produced and half of those seeds were sent back to Rodrigues to be used in restoration efforts. As of 2010, 300 of those seed have been germinated, opening up many more opportunities for reintroduction into the wild. Those early trials will set the stage for more restoration efforts in the future. It is rare that we see such an amazing success story when it comes to such an endangered species. We must celebrate these efforts because they remind us to keep trying even if all hope seems to be lost. My hat is off to Carlos and the dedicated team of plant conservationists and growers at Kew.

Photo Credits: [1] [2] [3] [4] [5]

Further Reading: [1] [2]

Meet the Pygmy Clubmoss

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No, these are not some sort of grass or rush. What you are looking at here is actually a member of the clubmoss family (Lycopodiaceae). Colloquially known as the pygmy clubmoss, this odd little plant is the only species in its genus - Phylloglossum drummondii. Despite its peculiar nature, very little is known about it.

The pygmy clubmoss is native to parts of Australia, Tasmania, and New Zealand but common it is not. From what I can gather, it grows in scattered coastal and lowland sites where regular fires clear the ground of competing vegetation. It is a perennial plant that makes its appearance around July and reaches reproductive size around August through to October.

Reproduction for the pygmy clubmoss is what you would expect from this family. In dividual plants will produce a reproductive stem that is tipped with a cone-like structure. This cone houses the spores, which are dispersed by wind. If a spore lands in a suitable spot, it germinates into a tiny gametophyte. As you can probably imagine, the gametophyte is small and hard to locate. As such, little is known about this part of its life cycle. Like all gametophytes, the end goal of this stage is sexual reproduction. Sperm are released and with any luck will find a female gametophyte and fertilize the ovules within. From the fertilized ovule emerges the sporophytes we see pictured above.

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As dormancy approaches, this strange clubmoss retreats underground where it persists as a tiny tuber-like stem. Though it is rather obscure no matter who you ask, there has been some scientific attention paid to this odd little plant, especially as it relates to its position on the tree of life. Since it was first described, its taxonomic affinity has moved around a bit. Early debates seemed to center around whether it belonged in Lycopodiaceae or its own family, Phylloglossaceae.

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Recent molecular work put this to rest showing that genetically the pygmy clubmoss is most closely related to another genus of clubmoss - Huperzia. This was bolstered by the fact that it shares a lot of features with this group such as spore morphology, phytochemistry, and chromosome number. The biggest difference between these two genera is the development of the pygmy clubmoss tuber, which is unique to this species. However, even this seems to have its roots in Lycopodiaceae.

If you look closely at the development of some lycopods, it becomes apparent that the pygmy clubmoss most closely resembles an early stage of development called the “protocorm.” Protocorms are a tuberous mass of cells that is the embryonic form of clubmosses (as well as orchids). Essentially, the pygmy clubmoss is so similar to the protocorm of some lycopods that some experts actually think of it as a permanent protocorm capable of sexual reproduction. Quite amazing if you ask me.

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Sadly, because of its obscurity, many feel this plant may be approaching endangered status. There have been notable declines in population size throughout its range thanks to things like conversion of its habitat to farmland, over-collection for both novelty and scientific purposes, and sequestration of life-giving fires. As mentioned, the pygmy clubmoss needs fire. Without it, natural vegetative succession quickly crowds out these delicate little plants. Hopefully more attention coupled with better land management can save this odd clubmoss from going the way of its Carboniferous relatives.

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

Further Reading: [1] [2] [3] [4] [5] [6]

On the Flora of Antarctica

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Antarctica - the frozen continent. It is hard to think of a place on Earth that is less hospitable to life. Yet life does exist here and some of it is botanical. Though few in number, Anarctica’s diminutive flora is able to eke out an existence wherever the right conditions present themselves. It goes without saying that these plants are some of the hardiest around.

It is strange to think of Antarctica as having any flora at all. How many descriptions of plant families and genera say something to the effect of “found on nearly every continent except for Antarctica.” It didn’t always used to be this way though. Antarctica was once home to a diverse floral assemblage that rivaled anything we see in the tropics today. Millions upon millions of years of continental drift has seen this once lush landmass positioned squarely at Earth’s southern pole.

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Situated that far south, Antarctica has long since become a frozen wasteland of sorts. The landscape is essentially a desert. Instead of no precipitation, however, most water in this neck of the woods is completely locked up in ice for most of the year. This is one reason why plants have had such a hard time making a living here. That is not to say that some plants haven’t made it. In fact, a handful of species thrive under these conditions.

When anyone goes looking for plants in Antarctica, they must do so wherever conditions ease up enough for part of the year to allow terrestrial life to exist. In the case of this frozen continent, this means hanging out along the coast or one of handful of islands situated just off of the mainland. Here, enough land thaws during the brief summer months to allow a few plant species to take root and grow.

Antarctic hair grass ( Deschamsia antarctica )

Antarctic hair grass (Deschamsia antarctica)

The flora of Antarctica proper consists of 2 flowering plant species, about 100 species of mosses, and roughly 30 species of liverwort. The largest of these are the flowering plants - a grass known as Antarctic hair grass (Deschamsia antarctica), and member of the pink family with a cushion-like growth habit called Antarctic pearlwort (Colobanthus quitensis). Whereas the hair grass benefits from being wind pollinated, the Antarctic pearlwort has had to get creative with its reproductive needs. Instead of relying on pollinators, which simply aren’t present in any abundance on Antarctica, it appears that the pearlwort has shifted over to being entirely self-pollinated. This seems to work for it because if the mother plant is capable of living on Antarctica, so too will its clonal offspring.

By far the dominant plant life on the continent are the mosses. With 100 species known to live on Antarctica, it is hard to make generalizations about their habits other than to say they are pretty tough plants. Most live out their lives among the saturated rocks of the intertidal zones. What we can say about these mosses is that they support a bewildering array of microbial life, from fungi and lichens to protists and tardigrades. Even in this frozen corner of the world, plants form the foundation for all other forms of life.

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Antarctic pearlwort ( Colobanthus quitensis )

Antarctic pearlwort (Colobanthus quitensis)

The coastal plant communities of Antarctica represent hotbeds of biodiversity for this depauperate continent. They reach their highest densities on the Antarctic Peninsula as well as on coastal islands such as south Orkney Islands and the South Shetland Islands. Here, conditions are just mild enough among the various rocky crevices for germination and growth to occur. Still, life on Antarctica is no cake walk. A short growing season, punishing waves, blistering winds, and trampling by penguins and seals present quite a challenge to Antarctica’s botanical denizens. They are able to live here despite these challenges.

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Still, humans take their toll. The Antarctic Peninsula is experiencing some of the most rapid warming on the planet over the last century. As this region grows warmer and drier each year, plants are responding accordingly. Antarctic mosses along the peninsula are increasingly showing signs of stress. They are starting to prioritize the production of protective pigments in their tissues over growth and reproduction. Moreover, new species of moss are starting to take over. Rapid warming and drying of the Antarctic Peninsula appears to be favoring species that are more desiccation tolerant at the expense of the continents endemic moss species.

Changes in the structure and composition of Antarctica’s moss beds is far from being a scientific curiosity for only bryologists to ponder. It is a symptom of greater changes to come.

Photo Credits: [1] [2] [3] [4] [5] [6]

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

Hydrostachyaceae: Enigmatic Rheophytes

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Today I would like to introduce you to an enigmatic family of aquatic angiosperms called Hydrostachyaceae. Though they kind of look like strange aquatic ferns or perhaps even lycopods, they are actually strange flowering plants. To find them, you need to hang out around waterfalls and rapids in either Madagascar or southern Africa.

Hydrostachyaceae is made up of roughly 22 species. This is a poorly understood group of plants and there is always a chance that more species await discovery. The various members of Hydrostachyaceae all take on a similar appearance. For much of the year they exist as a set of feathery, fern-like leaves that grow surprisingly large and look quite delicate, especially considering the types of habitats in which they grow.

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Their delicate appearance is deceptive. In fact, the feathery structure of their leaves is an adaptation to the waters in which they grow. These are plants that require fast moving, clean, fresh water. If they were to produce flat, unbroken leaves, the fast currents would quickly rip them to shreds. By producing long, feathery leaves, water simply flows right over them with minimal disturbance. However, their preferred habitats also make them extremely difficult to study. Hence we know very little about their ecology.

What we do know about these plants is that they need clean rock surfaces and clear water for germination and subsequent growth. Dump too much sediment in the stream and you can kiss these plants goodbye. When they dry season approaches and water levels begin to drop, these oddball plants go into flowering mode. To the best of my knowledge, nearly all members of this family are dioecious, meaning individual plants are either male or female. When it comes time to flower, each plant produces modest sized spikes densely packed with flower.

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The spikes themselves sit up and above the water line, which is how this family and genus got its name. Hydrostachys is Greek and roughly translates to “water spike.” I have not been able to track down any solid information on what might be pollinating these blooms, however, given their small, dense nature, and the extreme places in which they live, my bet would be on wind.

The ecology of Hydrostachyaceae isn’t the only mystery about these plants. Their position on the tree of life has also been cause for confusion ever since they were discovered. Morphologically speaking, aquatic angiosperms can offer a lot of confusion to taxonomists. Like whales, the ancestors of aquatic angiosperms lived out their lives on land. Making the move back into water comes with a lot of extremely specialized adaptations that can cloud our morphological interpretations of things.

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Some authors have put forth the idea that these plants belong to another family of highly derived aquatic angiosperms - the Podostemaceae. However, genetic analyses paint a much different story. When the Angiosperm Phylogeny Group got a hold of specimens, their molecular work suggested the Hydrostachyaceae were nestled in Cornales, somewhere near the Hydrangea family (Hydrangeaceae). Exactly where Hydrostachyaceae fits into this new classification is still up for debate but it just goes to show you how messy things can get when plant lineages return to water.

Sadly, like so many other plants, the various members of Hydrostachyaceae are under a lot of pressure in the wild. Basically anything that threatens the quality of streams and rivers is a threat to the ongoing survival of these species. Runoff pouring into water ways from agriculture and mining cloud up the water and bury available germination sites under layers of sediment. Things only get worse when hydroelectric projects are installed. The fate of these plants is unequivocally tied to water quality.

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Photo Credits: [1] [2] [3] [4] [5]

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

A Relictual Palm in the American Southwest

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Scattered throughout hidden oases nestled in the southwest corner of North America grows a glorious species of palm known to science as Washingtonia filifera. This charismatic tree goes by a handful of common names such as the desert fan palm, petticoat palm, and California fan palm. No matter what you call it, there is no denying that this palm is both unique and important to this arid region.

Populations of the desert fan palm are few and far between, occurring in a few scattered locations throughout the Colorado and Mojave Deserts. This palm can’t grow just anywhere in these deserts either. Instead, its need for water restricts it to small oases where springs, streams, or a perched water table can keep them alive.

Fossil evidence from Wyoming suggests that the restricted distribution of this palm is a relatively recent occurrence. Though not without plenty of debate, our current understanding of the desert fan palm is that it could once be found growing throughout a significant portion of western North America but progressive drying has seen its numbers dwindle to the small pockets of trees we know today.

The good news is that, despite being on conservation lists for its rarity, the desert fan palm appears to be expanding its range ever so slightly. One major component of this range expansion has to do with human activity. The desert fan palm makes a gorgeous specimen plant for anyone looking to add a tropical feel to their landscape. As such, it has been used in plantings far outside of its current range. Some reports suggest that it is even becoming naturalized in places like Death Valley, Sonoran Mexico, and even as far away as Florida and Hawai’i.

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Other aspects contributing to its recent range expansion are also attributable to human activity, though indirectly. For one, with human settlement comes agriculture, and with agriculture comes wells and other forms of irrigation. It is likely that the seeds of the desert fan palm can now find suitably wet areas for germination where they simply couldn’t before. Also, humans have done a great job at providing habitat for potential seed dispersers, especially in the form of coyotes and fruit-eating birds.

It’s not just an increase in seed dispersers that may be helping the desert fan palm. Pollinators may be playing a role in its expansion as well, though in a way that may seem a bit counterintuitive. With humans comes a whole slew of new plants in the area. This greatly adds to the floral resources available for insect pollinators like bees.

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Historically it has been noted that bees, especially carpenter bees, tend to be rather aggressive with palm inflorescences as they gather pollen, which may actually reduce pollination success. It is possible that with so many new pollen sources on the landscape, carpenter bees are visiting palm flowers less often, which actually increases the amount of pollen available for fertilizing palm ovules. This means that the palms could be setting more seed than ever before. Far more work will be needed before this mechanism can be confirmed.

Aside from its unique distribution, the desert fan palm has an amazing ecology. Capable of reaching heights of 80 ft. (25 m) or more and decked out in a skirt of dead fronds, the desert fan palm is a colossus in the context of such arid landscapes. It goes without saying that such massive trees living in desert environments are going to attract their fair share of attention. The thick skirt of dead leaves that cloaks their trunks serve as vital refuges for everything from bats and birds, to reptiles and countless of insects. Fibers from its leaves are often used to build nests and line dens.

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And don’t forget the fruit! Desert fan palms can produce copious amount of hard fruits in good years. These fruits go on to feed many animals. Coupled with the fact that the desert fan palm always grows near a water source and you can begin to see why these palms are a cornerstone of desert oases. There has been some concern over the introduction of an invasive red palm weevil (Rhynchophorus ferrugineus), however, researchers were able to demonstrate that the desert fan palm has a trick up its sleeve (leaf skirt?) for dealing with these pests.

It turns out that desert fan palms are able to kill off any of these weevils as they try to burrow into its trunk. The desert fan palm secretes a gummy resin into damaged areas, which effectively dissuaded most adults and killed off developing beetle larvae. For now it seems that resistance is enough to protect this palm from this weevil scourge.

It is safe to say that regardless of its limited distribution, the desert fan palm is one tough plant. Its towering trunks and large, fan-like leaves stand as a testament to the wonderful ways in which natural selection shapes organisms. It is a survivor and one that has benefited a bit from our obsession with cultivating palms.

Photo Credits: [1] [2] [3] [4] [5]

Further Reading: [1] [2] [3] [4] [5]


Are Packrats Fumigating Their Homes Using Plants?

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Any organism that lives in one place for a long enough time is going to have to deal with pests. For mammals, this often means fleas and ticks. Nests, dens, and other roosting spots tend to accumulate high numbers of these blood suckers the longer they are in use. As such, anything that can cut down on pest loads in and around the home has the potential to confer great advantages. Evidence from California suggests that wood rats may be using the leaves of a shrub to do just that.

Dusky-footed wood rats (A.K.A. packrats) build giant nests out of twigs and other plant debris. These nests serve to protect packrats from both the elements and hungry predators. Packrat nests can last for quite a long time and reach monumental proportions considering the size of the rat itself. Because they use these stick nests for long periods of time, it should come as no surprise that they can build up quite a pest load. Fleas are especially problematic for these rodents.

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A dusky-footed woodrat ( Neotoma fuscipes ) and its den.

A dusky-footed woodrat (Neotoma fuscipes) and its den.

When researchers took a closer look at what packrats were bringing into their nests, they realized that not all plant material was treated equally. Whereas packrats actively collect and feed on leaves from various oaks (Quercus spp.), conifers (Pinus spp., Juniperus spp., etc.), and toyon (Heteromeles arbutifolia), the packrats seemed to have a special affinity for the leaves of the California bay (Umbellularia californica). However, instead of taking huge bites out of bay leaves, the rats appear to nibble them along the margin and spread them throughout their nest. What’s more, fresh bay leaves are brought in every few days.

This led some researchers to suggest that, instead of packrats using bay leaves as food, they may be using them to fumigate their homes. Indeed, California bay is rather chemically active. It is an aromatic shrub noted for its resistance to insect infestation. Of special interest to the research team were a group of chemical compounds called monoterpenoids. They noted that bay leaves were especially high in two types of of these compounds - 1,8-cineole (which gives the shrub its characteristic odor), and umbellulone (which has shown to be quite toxic to rodents). Why else would packrats bring something potentially deadly into their home other than to drive off pests?

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Closer observation revealed that the packrats were in fact treating bay leaves differently than other leaves. For starters, bay leaves were disproportionately used to line the sleeping chambers within the stick nests. What’s more, the bay leaves were cycled out every 2 to 3 days. Even the nibbling patterns were significantly different. As mentioned above, bay leaves were merely nibbled along the leaf margins, which is an ideal place to nibble if releasing volatile compounds is the desired effect.

When researchers tested the effectiveness of a variety of leaves in the lab, their results added further evidence to the fumigation hypothesis. More than any other leaf found in packrat nests, bay leaves had clear negative effects on flea numbers. Flea survival in the lab was reduced by upwards of 75% when California bay leaves were present whereas flea survival was only reduced by less than 10% with all other leaves. It goes without saying that, whether they are conscious decisions or not, packrats definitely stand to benefit by decorating their homes with California bay leaves.

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

Further Reading: [1]

Arctic Vegetation is Growing Taller & Why That Matters

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The Arctic ecosystem is changing and it is doing so at an alarming rate. Indeed, the Arctic Circle is warming faster than most other ecosystems on this planet. All of this change has implications for the plant communities that call this region home. In a landmark study that incorporated thousands of data points from places like Alaska, Canada, Iceland, Scandinavia, and Russia, researchers have demonstrated that Arctic vegetation is, on average, getting taller.

Imagine what it is like to be a plant growing in the Arctic. Extreme winds, low temperatures, a short growing season, and plenty of snow are just some of the hardships that characterize life on the tundra. Such harsh conditions have shaped the plants of this region into what we know and love today. Arctic plants tend to hug the ground, hunkering down behind whatever nook or cranny offers the most respite from their surroundings. As such, plants of Arctic-type habitats tend to be pretty small in stature. As you can probably imagine, if these limits to plant growth become less severe, plants will respond accordingly.

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That is part of what makes this new paper so alarming. The vegetation that comprise these Arctic communities is nearly twice as tall today as it was 30 years ago. However, the increase in height is not because the plants that currently grow there are getting taller but rather because new plants are moving northwards into these Arctic regions. New players in the system are usually cause for concern. Other studies have shown that it isn’t warming necessarily that hurts Arctic and alpine plants but rather competition. They simply cannot compete as well with more aggressive plant species from lower latitudes.

Taller plants moving into the Arctic may have even larger consequences than just changes in species interactions. It can also change ecosystem processes, however, this is much harder to predict. One possible consequence of taller plants invading the Arctic involves carbon storage. It is possible that as conditions continue to favor taller and more woody vegetation, there could actually be more carbon storage in this system. Woody tissues tend to sequester more carbon and shading from taller vegetation may slow decomposition rates of debris in and around the soil.

Alopecurus alpinus  is one of the new tall plant species moving into the Arctic

Alopecurus alpinus is one of the new tall plant species moving into the Arctic

It is also possible that taller vegetation will alter snowpack, which is vital to the health and function of life in the Arctic. Taller plants with more leaf area could result in a reduced albedo in the surrounding area. Lowering the albedo means increased soil temperatures and reduced snowpack as a result. Alternatively, taller plants could also increase the amount of snowpack thanks to snow piling up among branches and leaves. This could very well lead (counterintuitively) to warmer soils and higher decomposition rates as snowpack acts like an insulating blanket, keeping the soil slightly above freezing throughout most of the winter.

It is difficult to make predictions on how a system is going to respond to massive changes in the average conditions. However, studies looking at how vegetation communities are responding to changes in their environment offer us one of the best windows we have into how ecosystems might change moving into the uncertain future we are creating for ourselves.

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

Further Reading: [1]

The Only True Cedars

Cedrus deodara

Cedrus deodara

The only true cedars on this planet can be found growing throughout mountainous regions of the western Himalayas and Mediterranean. All others are cedars by name only. The so-called “cedars” we encounter here in North America are not even in the same family as the true cedars. Instead, they belong to the Cypress family (Cupressaceae). The true cedars all belong to the genus Cedrus and are members of the family Pinaceae. They are remarkable trees with tons of ecological and cultural value.

J. White,1803-1824.

J. White,1803-1824.

The true cedars are stunning trees to say the least. They regularly reach heights of 100 ft. (30 m.) or more and can live for thousands of years. Cedars exhibit a dimorphic branching structure, with long shoots forming branches and smaller shoots carrying most of the needle load. The needles themselves are borne in dense, spiral clusters, giving the branches a rather aesthetic appearance. Each needle produces layers of wax, which vary in thickness depending on how exposed the tree is growing. This waxy layer helps protect the tree from sunburn and desiccation.

Cedrus libani

Cedrus libani

Cedrus libani

Cedrus libani

One of the easiest ways to identify a cedar is by checking out its cones. All members of the genus Cedrus produce upright, barrel-shaped cones. Male cones are smaller and don’t stay on the tree for very long. Female cones, on the other hand, are quite large and stay on the tree until the seeds are ripe. Upon ripening, the entire female cone disintegrates, releasing the seeds held within. Each seed comes complete with blisters full of distasteful resin, which is thought to deter seed predators.

Male cones of  Cedrus atlantica

Male cones of Cedrus atlantica

Female  Cedrus  cones.

Female Cedrus cones.

In total, there are only four recognized species of cedar - the Atlas cedar (Cedrus atlantica), the Cyprus cedar (C. brevifolia), the deodar cedar (C. deodara), and the Lebanon cedar (C. libani). I have heard arguments that C. brevifolia is no more than a variant of C. libani but I have yet to come across any source that can say this for certain. Much more work is needed to assess the genetic structure of these species. Even their place within Pinaceae is up for debate. Historically it seems that Cedrus has been allied with the firs (genus Abies), however, work done in the early 2000’s suggests that Cedrus may actually be sister to all other Pinaceae. We need more data before anything can be said with certainty.

Cedrus atlantica

Cedrus atlantica

Regardless, two of these cedars - C. atlantica & C. libani - are threatened with extinction. Centuries of over-harvesting, over-grazing, and unsustainable fire regimes have taken their toll on wild populations. Much of what remains is not considered old growth. Gone is the heyday of giant cedar forests. Luckily, many populations are now located in protected areas and reforestation efforts are being put into place throughout their range. Still, the ever present threat of climate change is causing massive pest outbreaks in these forests. The future for these trees hangs in the balance.

Photo Credit: Wikimedia Commons

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

Getting to Know Sansevieria

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The houseplant hobby is experiencing something of a renaissance as of late. With their popularity on various social media platforms, easy to grow plant species and their cultivars are experiencing a level of popularity they haven't seen in decades. One genus of particular interest to houseplant hobbyists is Sansevieria.

Despite their popularity, the few Sansevieria species regularly found in cultivation come attached with less than appealing common names. Mother-in-law's tongue, Devil's tongue, and snake plant all carry with them an air of negativity for what are essentially some of the most forgiving houseplants on the market. What few houseplant growers realize is that those dense clumps of upright striped leaves tucked into a dark corner of their home belong to a fascinating genus worthy of our admiration. What follows is a brief introduction to these enigmatic houseplants.

Sansevieria cylindrica

Sansevieria cylindrica

Sansevieria ballyi

Sansevieria ballyi

The Sansevieria we encounter in most nurseries are just the tip of the iceberg. Sansevieria is a genus comprise of about 70 different species. I say 'about' because this group is a taxonomic mess. There are a couple reasons for this. For starters, the vast majority of Sansevieria species are painfully slow growers. It can take decades for an individual to reach maturity. As such, they have never really presented nursery owners with much in the way of economic gain and thus only a few have received any commercial attention.

Another reason has to do with the fiber market during and after World War II. In hopes of discovering new plant-based fibers for rope and netting, the USDA collected many Sansevieria but never formally described most of them. Instead, plants were assigned numbers in hopes that future botanists would take the time needed to parse them out properly.

A third reason has to do with the variety of forms and colors these plants can take. Horticulturists have been fond of giving plants their own special cultivar names. This complicates matters as it is hard to say which names apply to which species. Often the same species can have different names depending on who popularized it and when.

Sansevieria grandis in situ .

Sansevieria grandis in situ.

Regardless of what we call them, all Sansevieria hail from arid regions of Africa, Madagascar and southern Asia. In the wild, many species resemble agave or yucca and, indeed, they occupy similar niches to these New World groups. Like so many other plants of arid regions, Sansevieria evolved CAM photosynthesis as a means of coping with heat and drought. Instead of opening up their stomata during the day when high temperatures would cause them to lose precious water, they open them at night and store CO2 in the form of an organic acid. When the sun rises the next day, the plants close up their stomata and utilize the acid-stored carbon for their photosynthetic needs.

The wonderfully compact  Sansevieria pinguicula .

The wonderfully compact Sansevieria pinguicula.

Often you will encounter clumps of Sansevieria growing under the dappled shade of a larger tree or shrub. Some even make it into forest habitats. Most if not all species are long lived plants, living multiple decades under the right conditions. These are just some of the reasons that they make such hardy houseplants.

The various Sansevieria appear the sort themselves out along a handful of different growth forms. The most familiar to your average houseplant enthusiast is the form typified by Sansevieria trifasciata. These plants produce long, narrow, sword shaped leaves that point directly towards the sky. Many other Sansevieria species, such as S. subspicata and S. ballyi, take on a more rosetted form with leaves that span the gamut from thin to extremely succulent. Still others, like S. grandis and S. forskaalii, produce much larger, flattened leaves that grow in a form reminiscent of a leaky vase. 

Sansevieria trifasciata  with berries .

Sansevieria trifasciata with berries.

Regardless of their growth form, a majority of Sansevieria species undergo radical transformations as they age. Because of this, adults and juveniles can look markedly different from one another, a fact that I suspect lends to some of the taxonomic confusion mentioned earlier. A species that illustrates this nicely is S. fischeri. When young, S. fischeri consists of tight rosettes of thick, mottled leaves. For years these plants continue to grow like this, reaching surprisingly large sizes. Then the plants hit maturity. At that point, the plant switches from its rosette form to producing single leaves that protrude straight out of the ground and can reach heights of several feet! Because the rosettes eventually rot away, there is often no sign of the plants previous form.

A young  Sansevieria fischeri  exhibiting its rosette form.

A young Sansevieria fischeri exhibiting its rosette form.

A mature  Sansevieria fischeri  with its large, upright, cylindrical leaves.

A mature Sansevieria fischeri with its large, upright, cylindrical leaves.

If patient, many of the Sansevieria will reach enormous sizes. Such growth is rarely observed as slow growth rates and poor housing conditions hamper their performance. It's probably okay too, considering the fact that, when fully grown, such specimens would be extremely difficult to manage in a home. If you are lucky, however, your plants may flower. And flower they do!

Though there is variation among the various species, Sansevieria all form flowers on either a simple or branched raceme. Flowers range in color from greenish white to nearly brown and all produce a copious amount of nectar. I have even noticed sickeningly sweet odors emanating from the flowers of some captive specimens. After pollination, flowers give way to brightly colored berries, hinting at their place in the family Asparagaceae.

A flowering  Sansevieria hallii .

A flowering Sansevieria hallii.

As a whole, Sansevieria can be seen as exceptional tolerators, eking out an existence wherever the right microclimate presents itself in an otherwise harsh landscape. Their extreme water efficiency, tolerance of shade, and long lived habit has lent to the global popularity of only a few species. For the majority of the 70 or so species in this genus, their painfully slow growth rates means that they have never made quite a splash in the horticulture trade.

Nonetheless, Sansevieria is one genus that even the non-botanically minded among us can pick out of a lineup. Their popularity as houseplants may wax and wane but plants like S. trifasciata are here to stay. My hope is that all of these folks collecting houseplants right now will want to learn more about the plants they bring into their homes. They are more than just fancy decorations, they are living things, each with their own story to tell. 

Photo Credits: [1] [2] [3] [4] [5] [6] [7] [8] [9]

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

Maples, Epiphytes, and a Canopy Full of Goodies

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The forests of the Pacific Northwest are known for the grandeur. This region is home to one of the greatest temperate rainforests in the world. A hiker is both dwarfed and enveloped by greenery as soon as they hit the trail. One aspect of these forests that is readily apparent are the carpets of epiphytes that drape limbs and branches all the way up into the canopy. Their arboreal lifestyle is made possible by a combination of mild winters and plenty of precipitation. 

Weare frequently taught that the relationship between trees and their epiphytes are commensal - the epiphytes get a place to live and the trees are no worse for wear. However, there are a handful of trees native to the Pacific Northwest that are changing the way we think about the relationship between these organisms in temperate rainforests.

Though conifers dominate the Pacific Northwest landscape, plenty of broad leaved tree species abound. One of the most easily recognizable is the bigleaf maple (Acer macrophyllum). Both its common and scientific names hint at its most distinguishing feature, its large leaves. Another striking feature of this tree are its epiphyte communities. Indeed, along with the vine maple (A. circinatum), these two tree species carry the greatest epiphyte to shoot biomass ratio in the entire forest. Numerous species of moss, liverworts, lichens, and ferns have been found growing on the bark and branches of these two species.

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Epiphyte loads are pretty intense. One study found that the average epiphyte crop of a bigleaf maple weighs around 78 lbs. (35.5 Kg). That is a lot of biomass living in the canopy! The trees seem just fine despite all of that extra weight. In fact, the relationship between bigleaf and vine maples and their epiphyte communities run far deeper than commensalism. Evidence accumulated over the last few decades has revealed that these maples are benefiting greatly from their epiphytic adornments.

Rainforests, both tropical and temperate, generally grow on poor soils. Lots of rain and plenty of biodiversity means that soils are quickly leached of valuable nutrients. Any boost a plant can get from its environment will have serious benefits for growth and survival. This is where the epiphytes come in. The richly textured mix of epiphytic plants greatly increase the surface area of any branch they live on. And all of that added surface area equates to more nooks and crannies for water and dust to get caught and accumulate.

When researchers investigated just how much of a nutrient load gets incorporated into these epiphyte communities, the results painted quite an impressive picture. On a single bigleaf maple, epiphyte leaf biomass was 4 times that of the host tree despite comprising less than 2% of the tree's above ground weight. All of that biomass equates to a massive canopy nutrient pool rich in nitrogen, phosphorus, potassium, calcium, magnesium, and sodium. Much of these nutrients arrive in the form of dust-sized soil particles blowing around on the breeze. What's more, epiphytes act like sponges, soaking up and holding onto precious water well into the dry summer months.

Now its reasonable to think that nutrients and water tied up in epiphyte biomass would be unavailable to trees. Indeed, for many species, epiphytes may slow the rate at which nutrients fall to and enter into the soil. However, trees like bigleaf and vine maples appear to be tapping into these nutrient and water-rich epiphyte mats.

A subcanopy of vine maple ( Acer circinatum ) draped in epiphytes.

A subcanopy of vine maple (Acer circinatum) draped in epiphytes.

Both bigleaf and vine maples (as well as a handful of other tree species) are capable of producing canopy roots. Wherever the epiphyte load is thick enough, bundles of cells just under the bark awaken and begin growing roots. This is a common phenomenon in the tropics, however, the canopy roots of these temperate trees differ in that they are indistinguishable in form and function from subterranean roots.

Canopy roots significantly increase the amount of foraging an individual tree can do for precious water and nutrients. Additionally, it has been found that canopy roots of the bigleaf maple even go as far as to partner with mycorrhizal fungi, thus unlocking even more potential for nutrient and water gain. In the absence of soil nutrient and water pools, a small handful of trees in the Pacific Northwest have unlocked a massive pool of nutrients located above us in the canopy. Amazingly, it has been estimated that mature bigleaf and vine maples with well developed epiphyte communities may actually gain a substantial fraction of their water and nutrient needs via their canopy roots.

 

Photo Credits: [1] [2]

Further Reading: [1] [2] [3] [4] [5]

 

The Plight of the African Violets

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For many of us, African violets (Saintpaulia spp.) are some of the first houseplants we learned how to grow. They are not true violets (Violaceae), of course, but rather members of the family Gesneriaceae. Nonetheless, their compact rosettes of fuzzy leaves coupled with regular sprays of colorful flowers has made them a multi-million dollar staple of the horticultural industry. Unfortunately their numbers in captivity overshadow a bleak future for this genus in the wild. Many African violets are teetering on the brink of extinction.

The genus Saintpaulia is endemic to a small portion of east Africa, with a majority of species being found growing at various elevations throughout the Eastern Arc Mountains of Kenya and Tanzania. Most of the plants we grow at home are clones and hybrids of two species, S. ionantha and S. confusa. Collected in 1892, these two species were originally thought to be the same species, S. ionantha, until a prominent horticulturist noted that there are distinct differences in the seed capsules each produced. Since the 1890's, more species have been discovered.

Saintpaulia goetzeana

Saintpaulia goetzeana

Exactly how many species comprise this genus is still up for some debate. Numbers range from as many as 20 to as few as 6. Much of the early work on describing various Saintpaulia species involved detailed descriptions of the density and direction of hairs on the leaves. More recent genetic work considers some of these early delineations to be tenuous at best, however, even these modern techniques have resolved surprisingly little when it comes to a species concept within this group.

Saintpaulia  sp.  in situ .

Saintpaulia sp. in situ.

Though it can be risky to try and make generalizations about an entire genus, there are some commonalities when it comes to the habitats these plants prefer. Saintpaulia grow at a variety of elevations but most can be found growing on rocky outcrops. Most of them prefer growing in the shaded forest understory, hence they do so well in our (often) poorly lit homes. Their affinity for growing on rocks means that many species are most at home growing on rocks and cliffs near streams and waterfalls. The distribution of most Saintpaulia species is quite limited, with most only known from a small region of forest or even a single mountain. Its their limited geographic distribution that is cause for concern.

Saintpaulia ionantha  subsp.  grotei in situ.

Saintpaulia ionantha subsp. grotei in situ.

Regardless of how many species there are, one fact is certain - many Saintpaulia risk extinction if nothing is done to save them. Again, populations of Saintpaulia species are often extremely isolated. Though more recent surveys have revealed that a handful of lowland species are more widespread than previously thought, mid to highland species are nonetheless quite restricted in their distribution. Habitat loss is the #1 threat facing Saintpaulia. Logging, both legal and illegal, and farming are causing the diverse tropical forests of eastern Africa to shrink more and more each year. As these forests disappear, so do Saintpaulia and all of the other organisms that call them home.

There is hope to be had though. The governments of Kenya and Tanzania have recognized that too much is being lost as their forests disappear. Stronger regulations on logging and farming have been put into place, however, enforcement continues to be an issue. Luckily for some Saintpaulia species, the type localities from which they were described are now located within protected areas. Protection coupled with inaccessibility may be exactly what some of these species need to survive. Also, thanks to the ease in which Saintpaulia are grown, ex situ conservation is proving to be a viable and valuable option for conserving at least some of the genetic legacy of this genus.

Saintpaulia intermedia

Saintpaulia intermedia

It is so ironic to me that these plants can be so common in our homes and offices and yet so rare in the wild. Despite their popularity, few recognize the plight of this genus. My hope is that, in reading this, many of you will think about what you can do to protect the legacy of plants like these and so many others. Our planet and the species that call it home are doomed without habitat in which to live and reproduce. This is why land conservation is an absolute must. Consider donating to a land conservation organization today. Here are two worth your consideration:

The Nature Conservancy

The Rainforest Trust

Photo Credits: [1] [2] [3] [4] [5]

Further Reading: [1] [2] [3] [4] [5]

The Carnivorous Dewy Pine

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The dewy pine is definitely not a pine, however, it is quite dewy. Known scientifically as Drosophyllum lusitanicum, this carnivore is odd in more ways than one. It is also growing more and more rare each year.

One of the strangest aspects of dewy pine ecology is its habitat preferences. Whereas most carnivorous plants enjoy growing in saturated soils or even floating in water, the dewy pine's preferred habitats dry up completely for a considerably portion of the year. Its entire distribution consists of scattered populations throughout the western Iberian Peninsula and northwest Morocco.

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Its ability to thrive in such xeric conditions is a bit of a conundrum. Plants stay green throughout the year and produce copious amounts of sticky mucilage as a means of catching prey. During the summer months, both air and soil temperatures can skyrocket to well over 100°F (37 °C). Though they possess a rather robust rooting system, dewy pines don't appear to produce much in the way of fine roots. Because of this, any ground water presence deeper in the soil is out of their reach. How then do these plants manage to function throughout the driest parts of the year?

During the hottest months, the only regular supply of water comes in the form of dew. Throughout the night and into early morning, temperatures cool enough for water to condense out of air. Dew covers anything with enough surface area to promote condensation. Thanks to all of those sticky glands on its leaves, the dewy pine possesses plenty of surface area for dew to collect. It is believed that, coupled with the rather porous cuticle of the surface of its leaves, the dewy pine is able to obtain water and reduce evapotranspiration enough to keep itself going throughout the hottest months. 

Dewy pine leaves unfurl like fern fiddle heads as they grow.

Dewy pine leaves unfurl like fern fiddle heads as they grow.

As you have probably guessed at this point, those dewy leaves do more than photosynthesize and collect water. They also capture prey. Carnivory in this species evolved in response to the extremely poor conditions of their native soils. Nutrients and minerals are extremely low, thus selecting for species that can acquire these necessities via other means. Each dewy pine leaf is covered in two types of glands: stalked glands that produce sticky mucilage, and sessile glands that secrete digestive enzymes and absorb nutrients.

Their ability to capture insects far larger than one would expect is quite remarkable. The more an insect struggles, the more it becomes ensnared. The strength of the dewy pines mucilage likely stems from the fact that the leaves do not move like those of sundews (Drosera spp.). Once an insect is stuck, there is not much hope for its survival. Living in an environment as extreme as this, the dewy pine takes no chances.

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The taxonomic affinity of the dewy pine has been a source of confusion as well. Because of its obvious similarity to the sundews, the dewy pine has long been considered a member of the family Droseraceae. However, although recent genetic work does suggest a distant relationship with Droseraceae and Nepenthaceae, experts now believe that the dewy pine is unique enough to warrant its own family. Thus, it is now the sole species of the family Drosophyllaceae.

Sadly, the dewy pine is losing ground fast. From industrialization and farming to fire suppression, dewy pines are running out of habitat. It is odd to think of a plant capable of living in such extreme conditions as being overly sensitive but that is the conundrum faced by more plants than just the dewy pine. Without regular levels of intermediate disturbance that clear the landscape of vegetation, plants like the dewy pine quickly get outcompeted by more aggressive plant species. Its the fact that dewy pine can live in such hostile environments that, historically, has kept its populations alive and well.

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What's more, it appears that dewy pines have trouble getting their seeds into new habitats. Low seed dispersal ability means populations can be cut off from suitable habitats that are only modest distances away. Without a helping hand, small, localized populations can disappear alarmingly fast. The good news is, conservationists are working hard on identifying what must be done to ensure the dewy pine is around for future generations to enjoy.

Changes in land use practices, prescribed fires, wild land conservation, and incentives for cattle farmers to adopt more traditional rather than industrial grazing practices may turn the table on dewy pine extinction. Additionally, dewy pines have become a sort of horticultural oddity over the last decade or so. As dedicated growers perfect germination and growing techniques, ex situ conservation can help maintain stocks of genetic material around the globe.

Photo Credits: [1] [2] [3] [4] [5]

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

 

 

Cycad Pollinators

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When it comes to insect pollination, flowering plants get all of the attention. However, flowers aren't the only game in town. More and more we are beginning to appreciate the role insects play in the pollination of some gymnosperm lineages. For instance, did you know that many cycad species utilize insects as pollen vectors? The ways in which these charismatic gymnosperms entice insects is absolutely fascinating and well worth understanding in more detail.

Cycads or cycad-like plants were some of the earliest gymnosperm lineages to arise on this planet. They did so long before familiar insects like bees, wasps, and butterflies came onto the scene. It had long been assumed that, like a vast majority of extant gymnosperms, cycads relied on the wind to get pollen from male cones to female cones. Indeed, many species certainly utilize to wind to one degree or another. However, subsequent work on a few cycad genera revealed that wind might not cut it in most cases.

White-haired cycad ( Encephalartos friderici-guilielm i)

White-haired cycad (Encephalartos friderici-guilielmi)

It took placing living cycads into wind tunnels to obtain the first evidence that something strange might be going on with cycad pollination. The small gaps on the female cones were simply too tight for wind-blown pollen to make it to the ovules. Around the same time, researchers began noting the production of volatile odors and heat in cycad cones, providing further incentives for closer examination.

Subsequent research into cycad pollination has really started to pay off. By excluding insects from the cones, researchers have been able to demonstrate that insects are an essential factor in the pollination of many cycad species. What's more, often these relationships appear to be rather species specific.

Cycadophila yunnanensis ,  C. nigra , and other beetles on a cone of  Cycas  sp.

Cycadophila yunnanensis, C. nigra, and other beetles on a cone of Cycas sp.

By far, the bulk of cycad pollination services are being performed by beetles. This makes a lot of sense because, like cycads, beetles evolved long before bees or butterflies. Most of these belong to the superfamily Cucujoidea as well as the true weevils (Curculionidae). In some cases, beetles utilize cycad cones as places to mate and lay eggs. For instance, male and female cones of the South African cycad Encephalartos friderici-guilielmi were found to be quite attractive to at least two beetle genera. 

Beetles and their larvae were found on male cones only after they had opened and pollen was available. Researchers were even able to observe adult beetles emerging from pupae within the cones, suggesting that male cones of E. friderici-guilielmi function as brood sites. Adult beetles carrying pollen were seen leaving the male cones and visiting the female cones. The beetles would crawl all over the fuzzy outer surface of the female cones until they became receptive. At that point, the beetles wriggle inside and deposit pollen. Seed set was significantly lower when beetles were excluded.

Male cone of  Zamia furfuracea  with a mating (lek) assembly of  Rhopalotria mollis  weevils.

Male cone of Zamia furfuracea with a mating (lek) assembly of Rhopalotria mollis weevils.

For the Mexican cycad Zamia furfuracea, weevils also utilize cones as brood sites, however, the female cones go to great lengths to protect themselves from failed reproductive efforts. The adult weevils are attracted to male cones by volatile odors where they pick up pollen. The female cones are thought to also emit similar odors, however, larvae are not able to develop within the female cones. Researchers attribute this to higher levels of toxins found in female cone tissues. This kills off the beetle larvae before they can do too much damage with their feeding. This way, the cycad gets pollinated and potentially harmful herbivores are eliminated. 

Beetles also share the cycad pollination spotlight with another surprising group of insects - thrips. Thrips belong to an ancient order of insects whose origin dates back to the Permian, some 298 million years ago. Because they are plant feeders, thrips are often considered pests. However, for Australian cycads in the genus Macrozamia, they are important pollinators.

Macrozamia macleayi  female cone.

Macrozamia macleayi female cone.

Thrip pollination was studied in detail in at least two Macrozamia species, M. lucida and M. macleayi. It was noted that the male cones of these species are thermogenic, reaching peak temperatures of around   104 °F (40 °C). They also produce volatile compounds like monoterpenes as well as lots of CO2 and water vapor during this time. This spike in male cone activity also coincides with a mass exodus of thrips living within the cones.

Thrips ( Cycadothrips chadwicki ) leaving a thermogenic pollen cone of  Macrozamia lucida.

Thrips (Cycadothrips chadwicki) leaving a thermogenic pollen cone of Macrozamia lucida.

Thrips apparently enjoy cool, dry, and dark places to feed and breed. That is why they love male Macrozamia cones. However, if the thrips were to remain in the male cones only, pollination wouldn't occur. This is where all of that male cone metabolic activity comes in handy. Researchers found that the combination of rising heat and humidity, and the production of monoterpenes aggravated thrips living within the male cones, causing them to leave the cones in search of another home.

Inevitably many of these pollen-covered thrips find themselves on female Macrozamia cones. They crawl inside and find things much more to their liking. It turns out that female Macrozamia cones do not produce heat or volatile compounds. In this way, Macrozamia are insuring pollen transfer between male and female plants.

Thrips up close.

Thrips up close.

Pollination in cycads is a fascinating subject. It is a reminder that flowering plants aren't the only game in town and that insects have been providing such services for eons. Additionally, with cycads facing extinction threats on a global scale, understanding pollination is vital to preserving them into the future. Without reproduction, species will inevitably fail. Many cycads have yet to have their pollinators identified. Some cycad pollinators may even be extinct. Without boots on the ground, we may never know the full story. In truth, we have only begun to scratch the surface of cycads and their pollinators.

Photo Credits: [1] [2] [3] [4] [5] [6] [7]

Further Reading: [1] [2] [3] [4] [5] [6]

Meet the Blazing Stars

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Midsummer in North America is, among other things, Liatris season. These gorgeous plants are often referred to as blazing stars or gayfeathers, which hints at the impact their flowers have on our psyche. Whether in the garden or in the wild, Liatris are a group of plants worth getting to know a bit better.

Liatris is by and large a North American genus with only a single species occurring in the Bahamas. Though we often think of Liatris as prairie plants, the center of diversity for this group is in the southeastern United States. Taxonomically speaking, Liatris are a bit of a conundrum. Something like 40 different species have been described and, where ranges overlap, many putative hybrids have been named.

Rocky Mountain blazing star ( Liatris ligulistylis )

Rocky Mountain blazing star (Liatris ligulistylis)

Authorities on this group cite ample confusion when it comes to drawing lines between species. Much of this confusion comes from the fact that numerous variants and intergradations exist between the various species. As mentioned, hybridization is not uncommon in this genus, which complicates matters quite a bit.

Prairie blazing star ( Liatris pycnostachya )

Prairie blazing star (Liatris pycnostachya)

Liatris as a whole appears to have undergone quite an adaptive radiation in North America, with species adapting to specific soils and habitat types. Take, for instance, the case of cylindrical blazing star (L. cylindracea), marsh blazing star (L. spicata), and rough blazing star (L. aspera). The ranges of these species overlap to quite a degree, however, each prefers to grow in soils of specific texture and moisture. Marsh blazing star, as you may have guessed, prefers wetter soils whereas rough blazing star enjoys drier habitats. Cylindrical blazing star seems to enjoy intermediate soil conditions, especially where soil pH is a bit higher. As such, these three species often occur in completely different habitats. However, in places like the southern shores of Lake Michigan, they find themselves growing in close quarters and as a result, a fair amount of hybridization has occurred.

Rough blazing star ( Liatris aspera )

Rough blazing star (Liatris aspera)

Another example of confusion comes from a species commonly known as the savanna blazing star (Liatris scariosa nieuwlandii). Many different ecotypes of this plant exist and some experts don't quite know how to deal with them all. Sometimes savanna blazing star is treated as a variant of another species called the northern blazing star (Liatris scariosa var. nieuwlandii) and sometimes it is treated as its own distinct species (Liatris nieuwlandii). Until proper genetic work can be done, it is impossible to say which, if any, are correct. 

Glandular blazing star ( Liatris glandulosa )

Glandular blazing star (Liatris glandulosa)

Taxonomic confusion aside, the various Liatris species and variants are important components of the ecology wherever they occur. Numerous insects feed upon and raise their young on the foliage and few could argue against their flowers as pollinator magnets. All Liatris produce pink to purple flowers in splendid Asteraceae fashion. Every once in a while, an aberrant form is produced that sports white flowers. Though horticulturists have capitalized on this for the garden, at least one authority claims that these white forms are much weaker than their pink flowering parents. At least one species, the pinkscale blazing star (L. elegans), produces large, filamentous white bracts that very much resemble flowers.

Check out the bracts on the pinkscale blazing star ( L. elegans )!

Check out the bracts on the pinkscale blazing star (L. elegans)!

Liatris are just as interesting below as they are above. The roots, foliage, and flowers all emerge from a swollen underground stem called a corm. The formation of these corms is one reason why some Liatris species have become so popular in our gardens. It makes them extremely hardy during the dormant season. In the spring, the corm starts forming roots. At the same time, tiny preformed buds at the top of the corm begin to grow this years crop of leaves and flowers. By the end of the growing season, the corm has reached its maximum size for that year and the plant draws down the rest of its reserves to wait out the winter.

Cylindrical blazing star ( Liatris cylindracea )

Cylindrical blazing star (Liatris cylindracea)

During this time, some species form a layer of tissue along the edge of the corm that is much darker in coloration than what was laid down earlier in the season. This has led some to suggest that aging individual Liatris is possible. Experts believe that specimens can readily reach 30 to 40 years of age or more, however, the degree to which these dark bands indicate annual growth is up for a lot of debate. Others have found no correlation with plant age. Regardless, it is safe to say that many Liatris species can live for decades if left undisturbed.

Scrub blazing star ( Liatris ohlingerae )

Scrub blazing star (Liatris ohlingerae)

All in all, Liatris is a very special, albeit slightly confusing, group of plants. It offers a little something for everyone. What's more, their beauty is only part of the story. These are ecologically important plants that support many great insect species. As summer wears on, make sure to get out there and enjoy the Liatris in your neck of the woods. You will be happy you did!

Photo Credits: [1] [2] [3] [4] [5] [6] [7] [8]

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