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]


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]

The Rose of Jericho

To survive in a desert, plants must eek out an existence in specific microclimates that provide conditions that are only slightly better than the surrounding landscape. Such is the case for the Rose of Jericho (Anastatica hierochuntica). This tenacious little mustard is found throughout arid regions of the Middle East and the Saharan Desert and it has been made famous the world over for its "resurrection" abilities. It is also the subject of much speculation so today we are going to separate fact from fiction and reveal what years of research has taught about this desert survivor. 

Natural selection has shaped this species into an organism fully ready to take advantage of those fleeting moments when favorable growing conditions present themselves. A. hierochuntica makes its living in dry channels called runnels or wadis, which concentrate water during periods of rain. It is a desert annual meaning the growth period of any individual is relatively short. Once all the water in the sandy soil has evaporated, this plant shrivels up and dies. This is not the end of its story though. With a little luck, the plants were pollinated and multiple spoon-shaped fruits have formed on its stems.

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As the dead husk of the plant starts to dry out, its branches curl up into a ball-like mass with most of the fruits tucked away in the interior. There the plant will sit, often for many years, until rain returns. When rain does finally arrive, things happen fast. After all, who knows how long it will be before it rains again. Thanks to a quirk of physiology, the dried tissues of A. hierochuntica are extremely elastic and can return to their normal shape and position once hydrated. As the soil soaks up water, the dried up stems and roots just under the surface also begin taking up water and the stems unfurl.

To call this resurrection is being a bit too generous. The plant is not returning to life. Instead, its dead tissues simply expand as they imbibe liquid. Water usually does not come to the desert without rain and rain is exactly what A. hierochuntica needs to complete its life cycle. Unfurling of its stems exposes its spoon-shaped fruits to the elements. Their convex shape is actually an adaptation for seed dispersal by rain, a mechanism termed ombrohydrochory. When a raindrop hits the fruit, it catapults the seed outward from the dead parent.

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If rains are light, seeds do not get very far. They tend to cluster around the immediate area of their parent. If rains are heavy, however, seeds can travel quite a distance. This is why one will only ever find this species growing in channels. During the rare occasions when those channels fill with water, seeds quickly float away on the current. In fact, experts believe that the buoyancy of A. hierochuntica seed is an adaptation that evolved in response to flooding events. It is quite ironic that water dispersal is such an important factor for a plant growing in some of the driest habitats on Earth.

To aid in germination, the seeds themselves are coated in a material that becomes mucilaginous upon wetting. When the seeds eventually come into contact with the soil, the mucilage sticks to the ground and causes the seeds to adhere to the surface upon drying. This way, they are able to effectively germinate instead of blowing around in the wind.

Again, things happen fast for A. hierochuntica. Most of its seeds will germinate within 12 hours of rainfall. Though they are relatively drought tolerant, the resulting seedlings nonetheless cannot survive without water. As such, their quick germination allows them to make the most out of fleeting wet conditions.

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Occasionally, the balled up husks of these plants will become dislodged from the sand and begin to blow around the landscape like little tumbleweeds. This has led some to suggest that A. hierochuntica utilizes this as a form a seed dispersal, scattering seeds about the landscape as it bounces around in the wind. Though this seems like an appealing hypothesis, experts believe that this is not the best means of disseminating propagules. Seeds dispersed in this way are much less likely to end up in favorable spots for germination. Though it certainly occurs, it is likely that this is just something that happens from time to time rather than something the plant has evolved to do.

In total, the Rose of Jericho is one tough cookie. Thanks to quick germination and growth, it is able to take advantage of those rare times when its desert environment become hospitable.

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

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

The Mystery of the Ghost Plant

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As houseplants enjoy a resurgence in our culture, untold numbers of novice and expert growers alike will have undoubtedly tried their luck at a succulent or two. Succulent, of course, is not a taxonomic division, but rather a way of describing the anatomy of myriad plants adapted to harsh, dry environments around the world. One of the most common succulents in the trade is the ghost plant (Graptopetalum paraguayense).

I would bet that, if you are reading this and you grow houseplants, you have probably grown a ghost plant at one point or another. They are easy to grow and will propagate a whole new plant from only a single leaf. Despite its worldwide popularity, the ghost plant is shrouded in mystery and confusion. To date, we know next to nothing about its ecology. Much of this stems from poor record keeping and the fact that we have no idea exactly where this species originated.

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That's right, we do not know the location of its native habitat. Records indicate that the first plants to find their way into human hands were imported into New York in 1904. Apparently, they were growing as "weeds" at the base of some South American cacti. Plants were lucky enough to wind up in the hands of competent botanists and the species has ended up with the name Graptopetalum paraguayense. The specific epithet "paraguayense" was an indication of much confusion to come as it was thought that the ghost plant originated in Paraguay.

Time has barely improved our knowledge. Considering many of its relatives hail from Mexico, it gradually became more apparent that South America could not claim this species as its own. Luck changed only relatively recently with the discovery of a population of a unique color variant of the ghost plant on a single mountain in northeastern Mexico. A thorough search of the area did not reveal any plants that resemble the plant so many of us know and love. It has been suggested that the original population from which the type species was described is probably growing atop an isolated mountain peak somewhere nearby in the Chihuahuan Desert.

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Despite all of the mystery surrounding this species, we can nonetheless elucidate some aspects about its biology by observing plants in cultivation. It goes without saying that the ghost plant is a species of dry, nutrient-poor habitats. Its succulence and tolerance of a wide array of soil conditions is a testament to its hardy disposition. Also, if plants are grown in full sun, they develop a bluish, waxy coating on their leaves. This is likely a form of sunscreen that the plant produces to protect it from sun scorch. As such, one can assume that its native habitat is quite sunny, though its ability to tolerate shade suggests it likely shares its habitat with shrubby vegetation as well. Given enough time and proper care, ghost plants will produce sprays of erect, 5 pointed flowers. It is not known who might pollinate them in the wild.

It is always interesting to me that a plant can be so well known to growers while at the same time being a complete mystery in every other way. A search of the literature shows that most of the scientific attention given to the ghost plant centers on potentially useful compounds that can be extracted from its tissues. Such is the case for far too many plant species, both known and unknown alike. Perhaps, in the not too distant future, some intrepid botanist will at last scramble up the right mountain and rediscover the original habitat of this wonderful plant. Until then, I hope this small introduction provides you with a new found appreciation for this wonderfully adaptable houseplant.

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

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

 

Meet the Ocotillo

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I love the ocotillo (Fouquieria splendens) for many reasons. It is an impossible plant to miss with its spindly, spine-covered stems. It is a lovely plant that is right at home in the arid parts of southwestern North America. Beyond its unique appearance, the ocotillo is a fascinating and important component of the ecology of this region.

My first impression of ocotillo was interesting. I could not figure out where this plant belonged on the tree of life. As a temperate northeasterner, one can forgive my taxonomic ignorance of this group. The family from which it hails, Fouquieriaceae, is restricted to southwestern North America. It contains one genus (Fouquieria) and about 11 species, all of which are rather spiky in appearance.

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Of course, those spines serve as protection. Resources like water are in short supply in desert ecosystems so these plants ensure that it is a real struggle for any animal looking to take a bite. Those spines are tough as well. One manged to pierce the underside of my boot during a hike and I was lucky that it just barely grazed the underside of my foot. Needless to say, the ocotillo is a plant worthy of attention and respect.

One of the most striking aspects of ocotillo life is how quickly these plants respond to water. As spring brings rain to this region of North America, ocotillo respond with wonderful sprays of bright red flowers situated atop their spindly stems. These blooms are usually timed so as to take advantage of migrating hummingbirds and emerging bees. The collective display of a landscape full of blooming ocotillo is jaw-droppingly gorgeous and a sight one soon doesn't forget. It is as if the whole landscape has suddenly caught on fire. Indeed, the word "ocotillo" is Spanish for "little torch."

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Flowering isn't the only way this species responds to the sudden availability of water. A soaking rain will also bring about an eruption of leaves, turning its barren, white stems bright green. The leaves themselves are small and rather fragile. They do not have the tough, succulent texture of what one would expect out of a desert specialist. That is because they don't have to ride out the hard times. Instead, ocotillo are what we call a drought deciduous species, producing leaves when times are good and water is in high supply, and dropping them as soon as the soil dries out.

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This cycle of growing and dropping leaves can and does happen multiple times per year. It is not uncommon to see ocotillo leaf out up to 4 or 5 times between spring and fall. During the rest of the year, ocotillo relies on chlorophyll in its stems for its photosynthetic needs. Interestingly enough, this poses a bit of a challenge when it comes to getting enough CO2. Whereas leaves are covered in tiny pours called stomata which help to regulate gas exchange, the stems of an ocotillo are a lot less porous, making it a challenge to get gases in and out. This is where the efficient metabolism of this plant comes in handy.

All plants undergo respiration like you and me. The carbohydrates made during photosynthesis are broken down to fuel the plant and in doing so, CO2 is produced. Amazingly, the ocotillo (as well as many other plants that undergo stem photosynthesis) are able to recycle the CO2 generated by cellular respiration back into photosynthesis within the stem. In this way, the ocotillo is fully capable of photosynthesis even without leaves.

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Through the good times and the bad, the ocotillo and its relatives are important components of desert ecology. They are as hardy as they are beautiful and getting to see them in person has been a remarkable experience. They ad a flare of surreality to the landscape that must be seen in person to believe.

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

The Mighty Saguaro Cactus

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Where does one begin with a plant like the saguaro cactus (Carnegiea gigantea)? It is recognized the world over for its iconic appearance yet its native range is disproportionately small compared to its popularity. It is easily one of the most spectacular plants I have ever encountered and I will never forget the sound the wind makes as it blows over its spiny pleated trunk. It would be impossible to sum up our collective knowledge of this species in one article, however, I feel that some form of an introduction is necessary. Today I want to honor this icon of the Sonoran Desert.

The saguaro is the only member of the genus Carnegiea, which is part of a subtribe of cacti characterized by their columnar appearance. Despite its unique taxonomic affinity, the evolutionary origins of this cactus remains a bit of a mystery. Though it is undoubtedly related to other columnar cacti of the Americas, a proper family tree seems to be just out of our reach. Due to lots of convergent and parallel evolution as well as conflicts between genealogies and species histories, we still aren't sure of its evolutionary origins. What we do know about this species on a genetic level is nonetheless quite interesting. For instance the saguaro has one of the smallest chloroplast genomes of any non-parasitic plant and we aren’t exactly sure why this is the case.

Saguaro are long lived cacti. Estimating age of a cactus can be rather tricky considering that they don’t produce annual growth rings. This is where long term monitoring projects have come in handy. By observing hundreds of saguaro throughout the Sonoran Desert, experts believe that saguaro can regularly reach ages of 150 to 170 years and some individuals may be able to live for more than 200 years. Amazingly, it is thought that saguaro will not begin to grow their characteristic arms until they reach somewhere around 50 to 100 years of age. That being said, some saguaro never bother growing arms. It all depends on where the conditions they experience throughout their lifetime.

Growth for a saguaro depends on where they are rooted. Under favorable conditions, a saguaro can grow to heights of 50 feet or more, with the world record holder clocking in at a whopping 78 feet in height. Such growth becomes all the more impressive when you realize just how agonizingly slow the process can be. Studies have shown that juvenile saguaro only put on about 1.5 inches of growth in their first eight years of life.

Despite preconceived notions about the hardy nature of most cacti, saguaro have proven to be rather specific in their needs. They are limited in their growth and distribution by the availability of water and warm temperatures. Saguaro, especially young individuals, cannot tolerate periods of prolonged frost. Additionally, germination and seedling survival occur most frequently only during the wettest years. In fact, one study showed that successful years for reproduction in these beloved cacti were tied to volcanic eruptions that cooled the climate just enough to allow the young saguaro to become established.

Outside of volcanic eruptions, saguaro appear to have friends in the surrounding vegetation. Studies have shown that saguaro seedlings seem to do best when growing under the shade of trees like the palo verde (Parkinsonia florida), ironwood (Olneya tesota), and mesquite (Prosopis velutina). The microclimates produced by these trees are much more favorable for saguaro growth than are open desert conditions. In essence, these trees serve as nurseries for young saguaro until they are large enough to handle more exposed conditions. Their nursery habits are not mutually beneficial however as research suggests that saguaro eventually compete with the trees that once protected them for precious resources like nutrients and water.

 Saguaros outgrowing their palo verde nurse tree. 

Saguaros outgrowing their palo verde nurse tree. 

At roughly 35 years of age, a saguaro will begin to flower. Flowers are small compared to the size of the cactus but they are abundant. Most flowers are produced at the apex of the cactus and it is thought that the growth of saguaro arms is largely a way of increasing the reproductive potential of large individuals. The flowers are cream colored and night scented. They open in the evening but will stay open and continue to produce nectar well into the morning hours.

Though a wide variety of animals will visit these flowers, the main pollinators are bees during the day and lesser long-nosed bats at night. Interestingly, it has been found that certain amino acids within the nectar of the saguaro can actually help female bats sustain lactation while raising their young, making them a valuable food source for these flying mammals. Catering to such a broad spectrum of potential pollinators is thought to have evolved as a means of increasing seed set. Each saguaro ovary contains many ovules and the more pollen that makes it onto the stigma, the more seeds will be produced.

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 A lesser long-nosed bat pollinates a saguaro bloom.

A lesser long-nosed bat pollinates a saguaro bloom.

Due to their size and abundance, it is easy to understand why the saguaro is such an ecologically important species in the Sonoran Desert ecosystem. In essence, they function similar to trees in that they serve as vital sources of shelter and food for myriad desert animals. Woodpeckers, especially the gila and the gilded flicker, regularly hollow out and build nests in saguaro trunks. These hollows are subsequently used by many different bird, mammal, and reptile species. The flowers and fruits are important sources of food for wildlife.

 Gila woodpecker with its nesting hole.

Gila woodpecker with its nesting hole.

 Gila woodpecker holes become homes for other birds like owls. 

Gila woodpecker holes become homes for other birds like owls. 

 On rare occasions, woodpecker holes can even become home to other cacti!

On rare occasions, woodpecker holes can even become home to other cacti!

I sincerely hope that this brief introduction does at least some justice to the wonderful organism that is the saguaro cactus. The Sonoran Desert would be a shell of an ecosystem without its presence. What’s more, it has played a significant role in the culture of this region for millennia. Though it appears quite numerous on the landscape, the long-term status of the saguaro is cause for concern. Numerous declines have been reported throughout its range. With its slow growth rates and infrequent recruitment events, the saguaro can be quite sensitive to rapid changes in its environment. Luckily it has received special protection laws throughout its US range.

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


Further Reading: [1] [2] [3] [4] [5] [6] [7] [8] [9] 

The Wild World of the Creosote Bush

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Apart from the cacti, the real rockstar of my Sonoran experience was the creosote bush (Larrea tridentata). Despite having been quite familiar with creosote as an ingredient, I admit to complete ignorance of the plant from which it originates. Having no familiarity with the Sonoran Desert ecosystem, I was walking into completely new territory in regard to the flora. It didn’t take long to notice creosote though. Once we hit the outskirts of town, it seemed to be everywhere.

If you are in the Mojave, Sonoran, and Chihuahuan Deserts of western North America, you are never far from a creosote bush. They are medium sized, slow growing shrubs with sprays of compact green leaves, tiny yellow flowers, and fuzzy seeds. Apparently what is thought of as one single species is actually made up of three different genetic populations. The differences between these has everything to do with chromosome counts. Populations in the Mojave Desert have 78 chromosomes, Sonoran populations have 52 chromosomes, and Chihuahuan have 26. This may have to do with the way in which these populations have adapted to the relative amounts of rainfall each of these deserts receive throughout the year, however, it is hard to say for sure.

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Regardless, creosote is supremely adapted to these xeric ecosystems. For starters, their branching architecture coupled with their tiny leaves are arranged so as to make the most out of favorable conditions. If you stare at these shrubs long enough, you may notice that their branches largely orient towards the southeast. Also, their leaves tend to be highly clustered along the branches. It is thought that this branching architecture allows the creosote to minimize water loss while maximizing photosynthesis.

Deserts aren’t hot 24 hours per day. Night and mornings are actually quite cool. By taking advantage of the morning sun as it rises in the east, creosote are able to open their stomata and commence photosynthesis during those few hours when evapotranspiration would be at its lowest. In doing so, they are able to minimize water loss to a large degree. Although their southeast orientation causes them to miss out on afternoon and evening sun to a large degree, the benefits of saving precious water far outweigh the loss to photosynthesis. The clustering of the leaves along the branches may also reduce overheating by providing their own shade. Coupled with their small size, this further reduces heat stress and water loss during the hottest parts of the day.

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Creosote also secrets lots of waxy, resinous compounds. These coat the leaves and to some extent the stems, making them appear lacquered. It is thought that this also helps save water by reducing water loss through the leaf cuticle. However, the sheer diversity of compounds extracted from these shrubs suggests other functions as well. It is likely that at least some of these compounds are used in defense. One study showed that when desert woodrats eat creosote leaves, the compounds within caused the rats to lose more water through their urine and feces. They also caused a reduction in the amount of energy the rats were able to absorb from food. In other words, any mammal that regularly feeds on creosote runs the risk of both dehydration and starvation. This isn’t the only interesting interaction that creosote as with rodents either. Before we get to that, however, we first need to discuss roots.

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Creosote shrubs have deep root systems that are capable of accessing soil water that more shallowly rooted plants cannot. This brings them into competition with neighboring plants in intriguing ways. When rainfall is limited, shallowly rooted species like Opuntia gain access to water before it has a chance to reach deeper creosote roots. Surprisingly this happens more often than you would think. The branching architecture of creosote is such that it tends to accumulate debris as winds blow dust around the desert landscape. As a result, the soils directly beneath creosote often contain elevated nutrients. This coupled with the added shade of the creosote canopy means that seedlings that find themselves under creosote bushes tend to do better than seedlings that germinated elsewhere. As such, creosote are considered nurse plants that actually facilitate the growth and survival of surrounding vegetation. So, if recruitment and resulting competition from vegetation can become such an issue for long term creosote survival, why then do we still so much creosote on the landscape?

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The answer may lie in rodents and other burrowing animals in these desert ecosystems. Take a look at the base of a large creosote and you will often find the ground littered with burrows. Indeed, many a mammal finds the rooting zone of the creosote shrub to be a good place to dig a den. When these animals burrow under shallowly rooted desert plants, many of them nibble on and disturb the rooting zones. Over the long-term, this can be extremely detrimental for the survival of shallow rooted species. This is not the case for creosote. Its roots run so deep that most burrowing animals cannot reach them. As such, they avoid most of the damage that other plants experience. This lends to a slight survival advantage for creosote at the expense of neighboring vegetation. In this way, rodents and other burrowing animals may actually help reduce competition for the creosote.

Barring major disturbances, creosote can live a long, long time. In fact, one particular patch of creosote growing in the Mojave Desert is thought to be one of the oldest living organisms on Earth. As creosote shrubs grow, they eventually get to a point in which their main stems break and split. From there, they begin producing new stems that radiate out in a circle from the original plant. These clones can go on growing for centuries. By calculating the average growth rate of these shrubs, experts have estimated that the Mojave specimen, affectionately referred to as the “King Clone,” is somewhere around 11,700 years old!

 The ring of creosote that is King Clone.

The ring of creosote that is King Clone.

For creosote, its slow and steady wins the race. They are a backbone of North American desert ecosystems. Their structure offers shelter, their seeds offer food, and their flowers support myriad pollinators. Creosote is one shrub worthy of our respect and admiration.

Photo Credit: [1] [2]

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

Palo Verde

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One of the first plants I noticed upon arriving in the Sonoran Desert were these small spiny trees without any leaves. The reason they caught my eye was that every inch of them was bright green. It was impossible to miss against the rusty brown tones of the surrounding landscape. It didn’t take long to track down the identity of this tree. What I was looking at was none other than the palo verde (Parkinsonia florida).

Palo verde belong to a small genus of leguminous trees. Parkinsonia consists of roughly 12 species scattered about arid regions of Africa and the Americas. The common name of “palo verde” is Spanish for “green stick.” And green they are! Like I said, every inch of this tree gives off a pleasing green hue. Of course, this is a survival strategy to make the most of life in arid climates.

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Despite typically being found growing along creek beds, infrequent rainfall limits their access to regular water supplies. As such, these trees have adapted to preserve as much water as possible. One way they do this is via their deciduous habit. Unlike temperate deciduous trees which drop their leaves in response to the changing of the seasons, palo verde drop their leaves in response to drought. And, as one can expect from a denizen of the desert, drought is the norm. Leaves are also a conduit for moisture to move through the body of a plant. Tiny pours on the surface of the leaf called stomata allow water to evaporate out into the environment, which can be quite costly when water is in short supply.

 The tiny pinnate leaves and pointy stems of the palo verde. 

The tiny pinnate leaves and pointy stems of the palo verde. 

Not having leaves for most of the year would be quite a detriment for most plant species. Leaves, after all, are where most of the photosynthesis takes place. That is, unless, you are talking about a palo verde tree. All of that green coloration in the trunk, stems, and branches is due to chlorophyll. In essence, the entire body of a palo verde is capable of performing photosynthesis. In fact, estimates show that even when the tiny pinnate leaves are produced, a majority of the photosynthetic needs of the tree are met by the green woody tissues.

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Flowering occurs whenever there is enough water to support their development, which usually means spring. They are small and bright yellow and a tree can quickly be converted into a lovely yellow puff ball seemingly overnight. Bees relish the flowers and the eventual seeds they produce are a boon for wildlife in need of an energy-rich meal.

However, it isn’t just wildlife that benefits from the presence of these trees. Other plants benefit from their presence as well. As you can probably imagine, germination and seedling survival can be a real challenge in any desert. Heat, sun, and drought exact a punishing toll. As such, any advantage, however slight, can be a boon for recruitment. Research has found that palo verde trees act as important nurse trees for plants like the saguaro cactus (Carnegiea gigantea). Seeds that germinate under the canopy of a palo verde receive just enough shade and moisture from the overstory to get them through their first few years of growth.

In total, palo verde are ecologically important trees wherever they are native. What’s more, their ability to tolerate drought coupled with their wonderful green coloration has made them into a popular tree for native landscaping. It is certainly a tree I won’t forget any time soon.

Further Reading: [1] [2]

The Pima Pineapple Cactus

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The Pima pineapple cactus (Coryphantha robustispina) is a federally endangered cactus native to the Sonoran Desert. It is a relatively small cactus by most standards, a fact that can make it hard to find even with a trained eye. Sadly, the plight of this cactus is shared by myriad other plant species of this arid region. Urbanization, fire, grazing, and illegal collection are an ever present threat thanks to our insatiable need to gobble up habitat we should never have occupied in the first place. 

Deserts are lands of extremes and the Pima pineapple cactus seems ready for whatever its habitat can throw its way (naturally). Plants are usually found growing individually but older specimens take on a clustered clonal habit. During the winter months, the Pima pineapple cactus shrivels and waits until warmth returns. Come spring, the Pima pineapple cactus begins anew. On mature specimens, flower buds begin to develop once the plant senses an increase in daylight. 

The flower buds continue to develop well into summer but seem to stop after a certain point. Then, with the onset of the summer monsoons, flower buds quickly mature and open all at once. It is thought that this evolved as a means of synchronizing reproductive events among widely spaced populations. You see, seed set in this species is best achieved via cross pollination. With such low numbers and a lot of empty space in between, these cacti must maximize the chances of cross pollination.

If they were to flower asynchronously, the chances of an insect finding its way to two different individuals is low. By flowering together in unison, the chances of cross pollination are greatly increased. No one is quite sure exactly how these cacti manage to coordinate these mass flowering events but one line of reasoning suggests that the onset of the monsoon has something to do with it. It is possible that as plants start to take up much needed water, this triggers the dormant flower buds to kick into high gear and finish their development. More work is needed to say for sure.

Seed dispersal for this species comes in the form of a species of hare called the antelope jackrabbit. Jackrabbits consume Pima fruits and disperse them across the landscape as they hop around. However, seed dispersal is just one part of the reproductive process. In order to germinate and survive, Pima pineapple cacti seeds need to end up in the right kind of habitat. Research has shown that the highest germination and survival rates occur only when there is enough water around to fuel those early months of growth. As such, years of drought can mean years of no reproduction for the Pima.

Taken together, it is no wonder then why the Pima pineapple cactus is in such bad shape. Populations can take years to recover if they even manage to at all. Sadly, humans have altered their habitat to such a degree that serious action will be needed to bring this species back from the brink of extinction. Aside from the usual suspects like habitat fragmentation and destruction, invasive species are playing a considerable role in the loss of Pima populations. 

Lehmann lovegrass (Eragrostis lehmanniana) was introduced to Arizona in the 1930's and it has since spread to cover huge swaths of land. What is most troubling about this grass is that it has significantly altered the fire regime of these desert ecosystems. Whereas there was once very little fuel for fires to burn through, dense stands of Lehmann lovegrass now offer plenty of stuff to burn. Huge, destructive fires can spread across the landscape and the native desert vegetation simply cannot handle the heat. Countless plants are killed by these burns.

Sometimes, if they are lucky, large cacti can resprout following a severe burn, however, all too often they do not. Entire populations can be killed by a single fire. What few plants remain are frequent targets of poaching. Cacti are quite a hit in the plant trade and sadly people will pay big money for rare specimens. The endangered status of the Pima pineapple cactus makes it a prized target for greedy collectors. 

The future of the Pima pineapple cactus is decidedly uncertain. Thankfully its placement on the endangered species list has afforded it a bit more attention from a conservation standpoint. Still, we know very little about this plant and more data are going to be needed if we are to develop sound conservation measures. This, my friends, is why land conservation is so important. Plants like the Pima pineapple cactus need places to grow. If we do not work harder on setting aside wild spaces, we will lose so much more than this species. 

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

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

The Strangest Wood Sorrel

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For me, wood sorrels are a group of plants I usually have to look down to find. This is certainly not the case for Oxalis gigantea. Native to the coastal mountains of northern Chile, this bizarre Oxalis has forgone the traditional herbaceous habit of its cousins in exchange for a woody shrub-like growth form.

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When I first laid eyes on O. gigantea, I thought I was looking at some strange form of Ocotillo. In front of me was a shrubby plant consisting of multiple upright branches that were covered in a dense layer of shiny green leaves occasionally interrupted by yellow flowers. You would think that at this point in my life, aberrant taxa would not longer surprise me. Think again. 

O. gigantea is one of the largest of the roughly 570 Oxalis species known to science. Its woody branches can grow to a height of 2 meters (6 feet)! The branches themselves are quite interesting to look at. They are covered in woody spurs from which clusters of traditional Oxalis-style leaves emerge. Each stem is capable of producing copious amounts of flowers all throughout the winter months. The flowers are said to be pollinated by hummingbirds but I was not able to find any data on this. 

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This shrub is but one part of the Atacama Desert flora. This region of Chile is quite arid,  experiencing a 6 to 10 month dry season every year. What rain does come is often sparse. Any plant living there must be able to cope. And cope O. gigantea does! This oddball shrub is deciduous, dropping its leaves during the dryer months. During that time, these shrubs look pretty ragged. You would never guess just how lush it will become once the rains return. Also, it has a highly developed root system, no doubt for storing water and nutrients to tide them over.  

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O. gigantea has enjoyed popularity as a horticultural oddity over the years. In fact, growing this shrub as a container plant is said to be quite easy. Despite its garden familiarity, O. gigantea is noticeably absent from the scientific literature. In writing this piece, I scoured the internet for any and all research I could find. Sadly, it simply isn't there.

This is all too often the case for unique and interesting plant species like O. gigantea. Like so many other species, it has suffered from the disdain academia has had for organismal research over the last few decades. We humans can and must do better than that. For now, what information does exist has come from horticulturists, gardeners, and avid botanizers from around the world. 

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

Further Reading: [1] [2] 

 

On the Ecology of Krameria

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There is something satisfying about saying "Krameria." Whereas so many scientific names act as tongue twisters, Krameria rolls of the tongue with a satisfying confidence. What's more, the 18 or so species within this genus are fascinating plants whose lifestyles are as exciting as their overall appearance. Today I would like to give you an overview of these unique parasitic plants.

Commonly known as rhatany, these plants belong to the family Krameriaceae. This is a monotypic clade, containing only the genus Krameria. Historically there has been a bit of confusion as to where these plants fit on the tree of life. Throughout the years, Krameria has been placed in families like Fabaceae and Polygalaceae, however, more recent genetic work suggests it to be unique enough to warrant a family status of its own. 

Regardless of its taxonomic affiliation, Krameria is a wonderfully specialized genus of plants with plenty of offer the biologically curious among us. All 18 species are shrubby, though at least a couple species can sometimes barely qualify as such. They are a New World taxon with species growing native as far south as Paraguay and Chile and as far north as Kansas and Colorado. They generally inhabit dry habitats.

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As I briefly mentioned above, most if not all of the 18 species are parasitic in nature. They are what we call "hemiparasites" in that despite stealing from their hosts, they are nonetheless fully capable of photosynthesis. It is interesting to note that no one has yet been able to raise these plants in captivity without a host. It would seem that despite being able to photosynthesize, these plants are rather specialized parasites. 

That is not to say that they have evolved to live off of a specific host. Far from it actually. A wide array of potential hosts, ranging from annuals to perennials, have been identified. What I find most remarkable about their parasitic lifestyle is the undeniable advantage it gives these shrubs in hot, dry environments. Research has found that despite getting a slow start on growing in spring, the various Krameria species are capable of performing photosynthesis during extremely stressful periods and for a much longer duration than the surrounding vegetation. 

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The reason for this has everything to do with their parasitic lifestyle. Instead of producing a long taproot to reach water reserves deep in the soil, these shrubs invest in a dense layer of lateral roots that spread out in the uppermost layers of soil seeking unsuspecting hosts. When these roots find a plant worth parasitizing, they grow around its roots and begin taking up water and nutrients from them. By doing this, Krameria are no longer limited by what water or other resources their roots can find. Instead, they have managed to tap into large reserves that would otherwise be locked away inside the tissues of their neighbors. As such, the Krameria do not have to worry about water stress in the same way that non-parasitic plants do. 

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By far the most stunning feature of the genus Krameria are the flowers. Looking at them it is no wonder why they have been associated with legumes and milkworts. They are beautiful and complex structures with a rather specific pollination syndrome. Krameria flowers produce no nectar to speak of. Instead, they have evolved alongside a group of oil-collecting bees in the genus Centris.

One distinguishing feature of Krameria flowers are a pair of waxy glands situated on each side of the ovary. These glands produce oils that female Centris bees require for reproduction. Though Centris bees are not specialized on Krameria flowers, they nonetheless visit them in high numbers. Females alight on the lip and begin scraping off oils from the glands. As they do this, they inevitably come into contact with the stamens and pistil. The female bees don't feed on these oils. Instead, they combine it with pollen and nectar from other plant species into nutrient-rich food packets that they feed to their developing larvae.  

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Following fertilization, seeds mature inside of spiny capsules. These capsules vary quite a bit in form and are quite useful in species identification. Each spine is usually tipped in backward-facing barbs, making them excellent hitchhikers on the fur and feathers of any animal that comes into contact with them.  

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

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

The Incredible Feat of a Resurrection Plant

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It is understandable why one would look at the crispy brown bundle of a Selaginella lepidophylla and think that it was dead. No wonder then why this hardy spikemoss has become such a novelty item for those looking for a unique gift. Indeed, even the common name of "resurrection plant" suggests that this species miraculously returns from the dead with the simple addition of water. A dormant resurrection plant is far from dead, however. It is in a state of dormancy that we are still struggling to understand.

Selaginella lepidophylla is native to the Chihuahuan desert, spanning the border between the US and Mexico. This is a harsh habitat for most plants, let alone a Lycophyte. However, this lineage has not survived hundreds of millions of years by being overly sensitive to environmental change and S. lepidophylla is a wonderful reminder of that.

As you can probably imagine, tolerating near-complete desiccation can be pretty beneficial when your habitat receives an average of only 235 mm (9.3 in) of rain each year. A plant can either store water for those lean times or go dormant until the rains return. The latter is exactly what S. lepidophylla does. As its water supply dwindles, the whole body of the plant curls up into a tight ball and waits. No roots anchor it to the ground. It is at the mercy of the winds as it blows around like a tiny tumbleweed until it winds up wedged into a crack or crevice.

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When the rains return, S. lepidophylla needs to be ready. Wet this crispy bundle and watch as over the course of about a day, the dormant ball unfurls to reveal the stunning body of a photosynthetic spikemoss ready to take advantage of moist conditions. Such conditions are short lived, of course, so after a few days drying out, the plant shrivels up and returns to its dormant, ball-like state. How does the plant manage to do this? Why doesn't it simply die? The answer to these questions has been the subject of quite a bit of debate and investigation. 

What we do know is that part of its success has to do with curling up into a ball. Without water in its tissues, its sensitive photosynthetic machinery would easily become damaged by punishing UV rays. By curling up, the plant essentially shelters these tissues from the sun. Indeed, plants that were kept from curling up experienced irreversible damage to their photo systems and were not as healthy as plants that did curl up. To this, the plant owes its success to rather flexible cell walls. Unlike other plants that snap when folded, the cells of S. lepidophylla are able to fold and unfold without any major structural damage.

As far as metabolism and chemistry is concerned, however, we are still trying to figure out how S. lepidophylla survives such drastic shifts. For a while it was thought that, similar to other organisms that undergo such dramatic desiccation, the plant relies on a special sugar called trehalose. Trehalose is known to bind to important proteins and membranes in other desiccation-tolerant organisms, thus protecting them from damage and allowing them to quickly return to their normal function as soon as water returns.

An analysis of non-desiccating Selaginella species, however, showed that S. lepidophylla doesn't produce a lot of trehalose. Though it is certainly present in its tissues, more wet-loving species of Selaginella contain much higher amounts of this sugar. Instead, it has been found that other sugars may actually be playing a bigger role in protecting the inner workings of this plant. Sorbitol and xylitol are found in much higher concentrations within the tissues of S. lepidophylla, suggesting that they may be playing a bigger role than we ever realized. More work is needed to say for sure.

Finally, it would appear that S. lepidophylla is able to maintain enzyme activities within its cells at much higher levels during desiccation periods than was initially thought possible. When dried, some enzymes were found to be working at upwards of 75% efficiency of those found in hydrated tissues. This is really important for a plant that needs to respond quickly to take advantage of fleeting conditions. Along with quick production of new enzymes, this "idling" of enzymatic activity during dormancy is thought to not only protect the plant from too much respiration, but also allows it to hit the ground running as soon as favorable conditions return. 

Despite our lack of understanding of the process, it is amazing to watch this resurrection plant in action. To see something go from a death-like state to a living, photosynthetic organism over the course of a day is truly a marvel worth enjoying.

Photo Credits: [1] [2]

Further Reading: [1]

In the Wake of Volcanoes

Recruitment windows are any period of time in which seeds germinate and grow into young plants successfully. Needless to say, they are a crucial component of of any plants' life cycle. For some species, these windows are huge, allowing them ample opportunity for successful reproduction. For others, however, these windows are small and specific. Take for instance the saguaro cactus (Carnegiea gigantea) of the American southwest. These arborescent cacti are famous the world over for their impressive stature. They are true survivors, magnificently adapted to their harsh, dry environment. This does not mean life is a cakewalk though. Survival, especially for seedlings, is measured by the slimmest of margins, with most saguaro dying in their first year. 

Hot, dry days and freezing cold nights are not particularly favorable conditions for young cacti. As such, any favorable change in weather can lead to much higher rates of successful recruitment for a given year. Because of this, saguaro often grow up as cohorts that all took advantage of the same favorable conditions that tipped the odds in their favor. This creates an age pattern that researchers can then use to better understand the population dynamics of these cacti. 

Recently, a researcher from York University noticed a particular pattern in the cacti she was studying. A large amount of the older cacti all dated back to the year 1884. What was so special about 1884, you ask? Certainly the climate must have been favorable. However, the real interesting part of this story is what happen the year before. 1883 saw the eruption of Krakatoa, a volcanic island located between Java and Sumatra. The eruption was massive, spewing tons of volcanic ash into the air. Effectively destroying the island, the eruption was so large that it was heard 1,930 miles away in western Australia. 

The effects of the Krakatoa eruption were felt worldwide. Ash and other gases spewed into the atmosphere caused a chilling of the northern hemisphere. Records of that time show an overall cooling effect of more than 2 degrees Fahrenheit. In the American Southwest, this led to record rainfall from July 1883 to June 1884. The combination of higher than average rainfall and lower than average temperatures made for a banner year for saguaro cacti. Seedlings were able to get past that first year bottleneck. After that first year, saguaro are much more likely to survive the hardships of their habitat. 

The Krakatoa eruption wasn't the only one with its own saguaro cohort. Further investigations have revealed similar patterns following the eruptions of Soufriere, Mt. Pelée, and Santa Maria in 1902, Ksudach in 1907, and Katmai in 1912. What this means is that conservation of species like the saguaro must take into account factors far beyond their immediate environment. Such patterns are likely not unique to saguaro either. The Earth functions as a biosphere and the lines we use to define the world around us can become quite blurry. If anything, this research underlines the importance of a system-based view. Nothing operates in a vacuum. 

Photo Credit: Geir K. Edland

Further Reading: [1] [2]

The Tumbleweed

What could be a more iconic symbol of the American West than the tumbleweed? From an early age we are indoctrinated with rustic images of tumbleweeds blowing across the high desert. But, did you know that there is very little about this iconic plant that could be considered American? That's right, our most common species of tumbleweed, Salsola tragus, is actually from Russia.

Salsola tragus, also known as Russian thistle, was accidentally introduced to South Dakota in the 1800's in a shipment of flaxseed. It is not actually a thistle at all but rather a member of the family Chenopodiaceae. Since then it has managed to spread throughout most of North America. In arid regions it has become quite a pest.

The tumbling aspect of its ecology has to do with seed dispersal. When the seeds mature, the plant dries up and breaks at the base. As the wind proceeds to blow the tumbleweed around it sprays seeds in every direction. Thanks to this novel method of seed dispersal it is easy to see how this plant is so common as to literally become synonymous with the American West. 

Photo Credit: VancityAllie

Further Reading:

http://1.usa.gov/1UiHDlR

http://bit.ly/1roOXSx

Velvet Turtleback

Death valley doesn't seem like a place where life would thrive. Nonetheless, a unique assemblage of plants can be found living in this hostile environment. These plants are well adapted to take advantage of those fleeting moments when things aren't so bad. A flush of flowers following a rare desert downpour is a reminder that even the harshest environments on this planet can harbor rich biodiversity. One of the coolest plants found in Death valley has to be the velvet turtleback (Psathyrotes ramosissima).

This peculiar little aster forms fuzzy little cushions that superficially resemble the domed shell of a turtle. The tightly packed leaves even give the appearance of scales. Everything about this plant is adapted to life in one of the driest places on Earth. For starters, it is a desert annual. Its seeds can lie dormant in the soil for many years until the perfect conditions arise. Once that happens, growth can be surprisingly rapid. In Death Valley, good conditions don't last long.

Even when conditions are right, its desert environment can still be quite challenging. Water loss and sun scorch are constant threats. Its cushion-like growth form and fuzzy leaves help reduce water loss as hot, dry winds whip across the region. The fuzzy leaves also help to reflect punishing UV rays that may otherwise fry the sensitive photosynthetic machinery inside.

All in all this is an incredible little plant. It survives in one of the toughest environments on the planet through a combination of timing and physiology. It is also but one of many desert-adapted species painting the valley during the brief growing season. As is typical of most of the plants of this region, its beauty is ephemeral and won't last much longer and to me, that makes it all the more wonderful.

Photo Credits: Stan Shebs and Dawn Endico - Wikimedia Commons

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