The Desert Mistletoe: Evolution In Action

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There are a multitude of mistletoes on this planet (for example: 1, 2, 3) and all of them are parasites to one degree or another. I find parasitic plants absolutely fascinating because there are as many variations on this lifestyle as there are hosts to parasitize. On a recent botanical adventure in the Sonoran Desert, I met yet another representative of this group - the desert mistletoe (Phoradendron californicum). Once I knew what I was looking at, I could not wait to do some research. As it turns out, this species has garnered quite a bit of attention over the years and it is teaching us some interesting tidbits on how parasites may evolve.

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The desert mistletoe is not hard to spot, especially during the driest parts of the year when most of its host trees have shed their leaves. It looks like a leafless, tangled mass of pendulous stems sitting among the branches of larger shrubs and trees. It can be found growing throughout both the Mojave and Sonoran deserts and appears to prefer leguminous trees including palo verde (Parkinsonia florida), mesquite (Prosopis spp.), and Acacia.

The desert mistletoe is a type of hemiparasite, which means it is capable of performing photosynthesis but nonetheless relies on its host tree for water and other nutrients. Lacking leaves, the desert mistletoe meets all of its photosynthetic needs via its green stems. Its leafless habit also makes its flowers and fruit all the more conspicuous. Despite their small size, its flowers are really worth closer inspection. When in bloom, a desert mistletoe comes alive with the hum of various insects looking for energy-rich nectar and pollen. Even before you spot them, you can easily tell if there is a blooming mistletoe nearby as the flowers give off a wonderfully sweet aroma. It appears that the desert mistletoe takes no chances when it comes to reproduction in such an arid climate.

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As I mentioned above, the desert mistletoe has been the subject of inquiry over the last few decades. Researchers interested in how parasitic plants evolve have illuminated some intriguing aspects of the biology of this species, especially as its relates to host preference. It would appear that our interest in this species seems to be situated at an important time in its evolutionary history. Not all populations of desert mistletoe "behave" in the same way. In fact, each seems to be heading towards more intense specialization based on its preferred host.

By performing seed transplant experiments, researchers have demonstrated that various populations of desert mistletoe seem to be specializing on specific tree species. For instance, when seeds collected from mistletoe growing on Acacia were placed on paleo verde or mesquite, they experienced significantly less germination than if they were placed on another Acacia. Though the exact mechanisms aren't clear at this point in time, evidence suggests that the success of desert mistletoe may be influenced by various hormone levels within the host tree, with isolated populations becoming more specialized on the chemistry of their specific host in that region.

Speaking of isolation, there is also evidence to show that populations of desert mistletoe growing on different host trees are reproductively isolated as well. Populations growing on mesquite trees flower significantly later than populations growing on Acacia or palo verde. Essentially this means that their genes never have the chance to mix, thus increasing the differences between these populations. Again, it is not entirely certain how the host tree may be influencing mistletoe flowering time, however, hormones and water availability are thought to play a role.

Another intriguing idea, and one that has yet to be tested, are the roles that seed dispersers may play in this evolutionary drama. After pollination, the desert mistletoe produces copious amounts of bright red berries that birds find irresistible. Two birds in particular, the northern mockingbird and the Phainopepla, aggressively defend fruiting mistletoe shrubs within their territories. It could be possible that these birds may be influencing which trees the seeds of the desert mistletoe end up on. Again, this is just a hypothesis but one that certainly deserves more attention.

A Phainopepla on the lookout for mistletoe berries.

A Phainopepla on the lookout for mistletoe berries.

Love them or hate them, there is something worth admiring about mistletoes. At the very least, they are important components of their native ecology. What's more, species like the desert mistletoe have a lot to teach us about the way in which species interact and what that means for biodiversity.

Photo Credit: [1]

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

Meet The Ghostworts

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I love parasitic plants and I love liverworts. Imagine my excitement then when I learned that there are at least two species of parasitic liverworts! These bizarre little plants are currently the only parasitic non-vascular plants known to science. 

The first description of a ghostwort dates back to 1919. Although no description of habitat was given, the account describes a set of liverwort thalli containing no chlorophyll and whose cells were full of mycorrhizal fungi. They were assigned to the genus Aneura and that was that. Further descriptions of this plant would not be made for more than a decade.

A ghostwort gametophyte with spike-like sporophytes.

A ghostwort gametophyte with spike-like sporophytes.

Proper attention was not given to this group until the 1930's. More plants started turning up among the humus and mosses of forests and wetlands throughout Finland, Sweden, and Scotland. A more thorough workover of specimens was made and the plants were moved into their own genus, Cryptothallus, which accurately captured their subterranean habit. They were given the name Cryptothallus mirabilis.

Another species of Cryptothallus was discovered in Costa Rica in 1977. It was named Cryptothallus hirsutus. Only one other collection of these species was made and it remains the lesser known of the two species. It is interesting to note the disparity between their ranges, with C. mirabilis inhabiting northern portions of Europe, and C. hirsutus only known from those two collections in Central America. Regardless, these odd liverworts have received a bit more attention in recent years.

It seems that the ghostworts manage to capture the attention of anyone who looks hard enough. For instance, a handful of attempts have been made to cultivate ghostworts in a controlled lab setting. Originally, plants were grown exposed to varying levels of light but try as the may, researchers were never able to coax the plants into producing chlorophyll. It would appear that these tiny liverworts are in fact some sort of parasite.

Spike-like sporophytes with a branching gametophyte. 

Spike-like sporophytes with a branching gametophyte. 

Proper evidence of their parasitic lifestyle was finally demonstrated 2003. Researchers were able to grow C. mirabilis in specialized observation chambers in order to understand what is going on under the soil. As it turns out, those numerous mycorrhizal connections mentioned in the original description are the key to survival for the ghostworts. The team showed that the ghostwort tricks fungi in the genus Tulasnella into forming mycorrhizal connections with its cells. These fungi also happen to be hooked up to a vast network of pine and birch tree roots.

By tricking the fungi, into an association, the ghostworts are able to steal carbohydrates that the fungi gain from the surrounding trees. Like all mycoheterotrophs, the ghostworts are essentially indirect parasites of photosynthetic plants. Their small size and relative rarity on the landscape likely helps these plants go unnoticed by the fungi but much more work needs to be done to better understand such dynamics.

Ghostworts look more like fungi than plants.

Ghostworts look more like fungi than plants.

In 2008, phylogenetic attention was paid to the ghostworts in order to better understand where they fit on the liverwort branch of the tree. As it turns out, Cryptothallus appears to be nestled quite comfortably within the genus Aneura. Because of this, the authors suggest disposing of the genus Cryptothallus altogether. Outside of simply placing this species back in its originally described genus, it affiliation with Aneura is quite interesting from an evolutionary standpoint.

Other liverworts in the genus Aneura are also known to form mycorrhizal relationships with Tulasnella. Unlike the ghostworts, however, these liverworts are fully capable of photosynthesis. Because these intimate fungal relationships were already in place before the ghostworts began evolving towards a fully parasitic lifestyle, it suggests that the saprophytic nature of Tulasnella fungi may have actually facilitated this jump. 

The cryptic nature of the ghostworts has left many a botanist wanting. Their subterranean habit makes them incredibly hard to find. Who knows what secrets this group still holds. Future discoveries could very well add more species to the mix or, at the very least, greatly expand the known range of the other two.

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

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

 

A Peculiar Parasite at Berkeley

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Parasitic plants are fascinating. I never pass up an opportunity to meet them. On a recent trip to California, my host for the day mentioned that something funny was growing in a patch of ivy on the Berkeley Campus. I had to know what it was. We took a detour from our intended rout and there, growing underneath a pine tree in a dense patch of ivy were these odd purple and brown stalks. This was definitely a parasitic plant.

The plant in question was the ivy broomrape (Orobanche hederae). As both its common and scientific name suggests, it is a parasite on ivy (Hedera spp.). As you can probably guess based on the identity of its host, ivy broomrape is not native to North America. In fact, the population we were looking at is the only known population of this plant you will find in the Americas. How it came to be in that specific location is a bit of a mystery but the proximity to the life sciences building suggests that this introduction might have been intentional. Personally I am quite alright with this introduction as it is parasitizing one of the nastier invasive species on this continent.

The ivy broomrape starts its life as a tiny seed. Upon germination, the tiny embryo sends out a thin thread-like filament that spirals out away from the embryo into the surrounding soils. The filament is looking for the roots of its host. Upon contact with ivy roots, the filament penetrates xylem tissues. The ivy broomrape is now plugged in, receiving all of its water, nutrient, and carbohydrate needs from the ivy. At this point the embryo begins to grow larger, throwing out more and more parasitic roots in the process. These locate more and more ivy roots until the needs of the ivy broomrape are met. Of course, all of this is going on underground.

Only when the ivy broomrape has garnered enough energy to flower will you see this plant. A stalk full of purple tinged, tubular flowers emerges from the ground. At this point its membership in the family Orobanchaceae is readily apparent. Like all members of this family, its parasitic lifestyle is so complete that it is beginning to lose genes for the production of chlorophyll and Rubisco, all things we generally associate with plants. This is why I love parasites so much. Not only are their ecological impacts bewilderingly complex, their evolutionary histories are such a departure from the norm. I will never tire of appreciating such species and I am happy to have met yet another awesome member of this group.

Further Reading:
http://onlinelibrary.wiley.com/doi/10.1111/j.1469-8137.1925.tb06671.x/pdf

http://cat.inist.fr/?aModele=afficheN&cpsidt=4107447

Newly Discovered Orchid Doesn't Bother With Photosynthesis or Opening Its Flowers

A new species of orchid has been discovered on the small Japanese island of Kuroshima. Though not readily recognized as an orchid, it nonetheless resides in the tribe Epidendroideae. Although the flowers of its cousins are often quite showy, this orchid produces small brown blooms that never open. What's more, it has evolved a completely parasitic lifestyle. 

The discovery of this species is quite exciting. The flora of Japan has long thought to be well picked over by botanists and ecologists alike. Finding something new is a special event. The discovery was made by Suetsugu Kenji, associate professor at the Kobe University Graduate School of Science. This discovery was made about a year after a previous parasitic plant discovery made on another Japanese island a mere stones throw from Kuroshima (http://bit.ly/2dYN12L).

Coined Gastrodia kuroshimensis, this interesting little parasite flies in the face of what we generally think of when we think of orchids. It is small, drab, and lives out its entire life on the shaded forest floor. Like the rest of its genus, G. kuroshimensis is mycoheterotrophic. It produces no leaves or chlorophyll, living its entire life as a parasite on mycorrhizal fungi underground. This is not necessarily bizarre behavior for orchids (and plants in general). Many different species have adopted this strategy. What was surprising about its discovery is the fact that its flowers never seem to open. 

In botany this is called "cleistogamy." It is largely believed that cleistogamy evolved as both an energy saving and survival strategy. Instead of dumping lots of energy into producing large, showy flowers to attract pollinators, that energy can instead be used for seed production and persistence. Additionally, since the flowers never open, cross pollination cannot occur. The resulting offspring share 100% of their genes with the parent plant. Although this can be seen as a disadvantage, it can also be an advantage when conditions are tough. If the parent plant is adapted to the specific conditions in which it grows, giving 100% of its genes to its offspring means that they too will be wonderfully adapted to the conditions they are born into. 

As you can probably imagine, pure cleistogamy can be quite risky if conditions rapidly change. In the face of continued human pressures and rapid climate change, cleistogamy as a strategy might not be so good. That is one reason why the discovery of this bizarre little orchid is so interesting. Whereas most species that produce cleistogamous flowers also produce "normal" flowesr that open, this species seems to have given up that ability. Thus, G. kuroshimensis offers researchers a window into how and why this reproductive strategy evolved. 

Photo Credit: Suetsugu Kenji

Further Reading:

[1]

The Largest Single Flower in the World

To find some of the largest flowers in the world, one must find themselves hiking through the the humid jungles of southeast Asia. From there you must be lucky enough to stumble across the flowers of a genus known scientifically as Rafflesia. It contains roughly 28 species spattered about various tropical islands. If you are very lucky, you might even find Rafflesia arnoldii. Producing flowers that are over 3 feet (1 m) in diameter and weighing as much as 24 pounds (11 kg), it produces the largest individual flower on the planet. 

Even more bizarre, these plants are entirely parasitic. They belong to a specialized group called holoparasites. These plants produce no stems, no leaves, nor any true roots. Their entire existence depends on a group of vines related to North America's grapes. Except for flowering, individual Rafflesia exist entirely as a network of mycelium-like cells inside the tissues of their vine hosts.


For a long time, the taxonomic status of this plant was highly debated but recent DNA evidence puts it in the order Malpighiales. From there, things get a little funny. One recent analysis suggested that Rafflesia belonged in the family Euphorbiaceae, however, it most likely warrants its own family - Rafflesiaceae.

So, why produce such large flowers? Well, existing solely within a vine makes it hard to establish a large population in any given area. This makes for a difficult situation in the pollinator department. Somehow plants must increase the odds that any given pollinator will visit multiple unrelated individuals of that particular species. By growing very large and and producing a lot of "stink" (this plant is also referred to as the corpse plant), Rafflesia make sure that pollinators will come from far and wide to investigate, thus increasing their chances of cross pollinating. How this plant goes about seed dispersal, however, remains a mystery.

Most interesting of all, it has been discovered that there is some amount of horizontal gene transfer going on between Rafflesia and its host. Basically, Rafflesia obtains strands of DNA from the vine and uses them in its own genetic code. It is believed this incurs some fitness benefit to Rafflesia but more research is needed to figure out why this may be happening. 

Sadly, many species within this family may be lost before we ever get a chance to get to know them. Forests throughout this region are disappearing rapidly to make room for expanding populations and agriculture. What makes matters worse for Rafflesia is that their lifestyle makes them very hard to study. It is especially difficult to obtain accurate population estimates. As more and more forests are cleared, we could be losing countless populations of these wonderful and intriguing plants. As with large mammals, it would seem that the world's largest flower is falling victim to the unending tide of human development. 

Photo Credit: Tamara van Molken


Further Reading:

http://bit.ly/2c2ALHl

http://bit.ly/2cPMP51

http://bit.ly/2cwP7ny

Rhizanthes lowii

Imagine hiking through the forests of Borneo and coming across this strange object. It's hairy, it's fleshy, and it smells awful. With no vegetative bits lying around, you may jump to the conclusion that this was some sort of fungus. You would be wrong. What you are looking at is the flower of a strange parasitic plant known as Rhizanthes lowii.

R. lowii is a holoparasite. It produces no photosynthetic tissues whatsoever. In fact, aside from its bizarre flowers, its doesn't produce anything that would readily characterize it as a plant. In lieu of stems, leaves, and roots, this species lives as a network of mycelium-like cells inside the roots of their vine hosts. Only when it comes time to flower will you ever encounter this species (or any of its relatives for that matter).

The flowers are interesting structures. Their sole purpose, of course, is to attract their pollinators, which in this case are carrion flies. As one would imagine, the flowers add to their already meaty appearance a smell that has been likened to that of a rotting corpse. Even more peculiar, however, is the fact that these flowers produce their own heat. Using a unique metabolism, the flower temperature can rise as much as 7 degrees above ambient. Even more strange is the fact that the flowers seem to be able to regulate this temperature. Instead of a dramatic spike followed by a gradual decrease in temperature, flowers are able to maintain this temperature gradient throughout the flowering period.

There could be many reasons for doing this. It could enhance the rate of floral development. This is a likely possibility as temperature increases have been recorded during bud development. It could also be used as a way of enticing pollinators, which can use the flower to warm up. This seems unlikely given its tropical habitat. Another possibility is that it helps disperse its odor by volatilizing the smelly compounds. In a similar vein, it may improve the carrion mimicry. Certainly this may play a role, however, flies don't seem to have an issue finding carrion that has cooled to ambient temperature. Finally, it has also been suggested that the heat may improve fertilization rates. This also seems quite likely as thermoregulation has been shown to continue after the flowers have withered away.

Regardless of its true purpose, the combination of lifestyle, appearance, and heat producing properties of this species makes for a bizarrely spectacular floral encounter. To see this plant in the wild would be a truly special event.

Photo Credit: Ch'ien C. Lee - www.wildborneo.com.my/photo.php?f=cld1500900.jpg

Further Reading:

http://www.jstor.org/stable/4222678?seq=1#page_scan_tab_contents

http://www.people.fas.harvard.edu/~ccdavis/pdfs/Nikolov_et_al_AJB_2014.pdf

Rusty Mustards

 

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Believe it or not, what you are seeing here is the same species of plant. The one on the left is the normal reproductive state of an Arabis mustard while the one on the right is the same species of mustard that has been infected by a rust fungus known as Puccinia monoica.

The interaction of these two species is interesting on so many levels. I spent an entire summer, along with my botanical colleagues, completely stumped as to what this strange orange-colored plant could be only to eventually find out that it was a mustard that has been hijacked! The fungus in question, Puccinia monoica, is part of a large complex of interrelated rust fungi who are quite fond of mustards. They utilize such an elaborate form of sexual reproduction.

The life cycle is as follows: Fungal spores land on a young mustard plant and begin to invade the host tissue. As they grow, they gain more and more nutrients from the mustard. Eventually the fungi effectively neuters its host and causes it to begin forming what are referred to as "pseudoflowers." The pseudoflowers are basically leaves that have been mutated by the fungus to look and smell a lot like other plants blooming in early summer. They produce a sticky, nectar-like substance that smells quite nice to pollinators. The mimicry even goes as far as to produce yellowish pigments that reflect UV light, making them an even more attractive target for passing insects. On each pseudoflower are hundreds of small cups known as spermatogonia. These house the sex cells of the fungus. The insect becomes covered in these sex cells, which it then transfers to other infected plants thus achieving sexual reproduction for Puccinia monoica.

Still with me?

At this point, the pseudoflowers stop producing color and nectar and instead, the fused sex cells germinate into hyphae that begin to form specialized structures called "aecia." The aceia house the spores that will be responsible for infecting their secondary host plants, which are grasses. The spores germinate and infect the grass. From there, structures called "uredia" are formed that go on to produce even more spores to infect even more grass. Eventually, structures called "telia" are formed on the grass and the cycle finally comes full circle. The telia produce the spores that will infect the original mustard host plants.

Whew! To have stumbled across an evolutionary drama such as this serves as a reminder of just how much in nature goes largely unnoticed every day.  

Further Reading:

http://onlinelibrary.wiley.com/doi/10.1046/j.1365-294x.1998.00426.x/abstract

http://www.sciencedirect.com/science/article/pii/0169534794901546

http://www.nature.com/nature/journal/v362/n6415/abs/362056a0.html

http://www.jstor.org/discover/10.2307/3761326?uid=3739256&sid=21102184095601

Flowers of the Underworld

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New Zealand has some weird nature. It is amazing to see what an island free of any major terrestrial predators can produce. Unfortunately, ever since humans found their way to New Zealand, the unique ecology has suffered. One of the most unique plant and animal interactions in the world can be found on this archipelago, but for how much longer is the question.

The story will start with a species of bat. In fact, this bat is New Zealand's only native terrestrial mammal. That's right, I said terrestrial. The New Zealand lesser short-tailed bat spends roughly 40% of its time foraging for insects on the ground. It has lots of specialized adaptations that I won't go into here but the cool part is these bats forage in packs, stirring up insects from the leaf litter until they reach a level of feeding frenzy that I thought was reserved only for sharks or piranhas. Along with using echo location, they also have a highly developed sense of smell. This is important for our second player in this forest drama. 

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Enter Dactylanthus taylorii, the wood rose. This plant is not a rose at all but rather a member of the tropical family Balanophoraceae. More importantly, it is parasitic. It produces no chlorophyll and lives most of it's life underground, wrapped around the roots of its host tree. Every once in a while a small patch of flowers breaks through the dirt and just barely rises above the leaf litter. This gives this species its Māori name of pua o te reinga or pua reinga, which translates to "flower of the underworld." The flowers emit a musky, sweet smell that attracts the ground foraging bats.

The bats are one of the only pollinators left for the wood rose. They sniff out the flowers and dine on the nectar, all the while being dusted with pollen. Recently, it has been found that New Zealand's giant ground parrot, the kakapo, is also believed to have been a pollinator of this plant. Sadly, the kakapo only exists on some of the smaller islands of the archipelago.

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Both the wood rose and the New Zealand lesser short-tailed bat are considered at risk of extinction. When modern man came to these islands they brought with them the general suite of mammalian invasives like rats, mongoose, cats, and pigs, all of which are exacting a major toll on the native ecology. The plants and animals of New Zealand have not shared an evolutionary history with such aggressive mammalian invaders and thus have no adaptations for coping with their sudden presence. The future of the wood rose, the New Zealand lesser short-tailed bat, and the kakapo, along with many other uniquely New Zealand species are for now uncertain.

Photo Credits: Joseph Dalton Hooker (1859), Wikimedia Commons, and Nga Manu Nature Reserve (http://www.ngamanu.co.nz/)

Further Reading:

http://phys.org/news/2012-10-flightless-parrots-burrowing-parasitic-hades.html

http://www.doc.govt.nz/documents/science-and-technical/Sfc019.pdf

http://www.edgeofexistence.org/mammals/species_info.php?id=56

Sandfood

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Pholisma is yet another amazing genus of parasitic plants. Endemic to the southwestern United States and Mexico, these peculiar members of the borage family tap into the roots of a variety of plant species. They do not photosynthesize and therefore obtain all the nutrients they need from their hosts. Oddly enough, researchers have found that most of their water needs are met by absorbing dew through the stomata on their highly reduced, scale-like leaves. Water is then stored in their highly succulent stems. Throughout their limited range, Pholisma are critically imperiled. Development and agriculture have already eliminated many populations. To add insult to injury, the dunes in which most extant populations are found are owned by the BLM and are open to heavy off-road ATV traffic, which will likely push them to the brink of extinction if nothing is done to limit such recreational use. Unless people speak up about protecting these plants and their habitats, they could disappear for good.

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Photo Credits: [1] [2] [3]

Further Reading: [1] [2]

The Holoparasitic Mistletoes

Flowers of   Tristerix aphyllu s

Flowers of Tristerix aphyllus

The order collectively referred to as mistletoes is incredibly diverse. They range in size from rather large trees down to little more than a couple leaves, barely recognizable on their hosts. Even more unique are the mistletoes that have foregone much of what we would readily recognize as an actual plant. These parasitic plants have adopted an endophytic lifecycle, living their entire lives within the vascular tissues of their host plants, only visible to observers when in flower. 

Tristerix aphyllus is one such species. Its hosts are cacti in the genus Echinopsis (formerly Trichocereus) native to Columbia and Chile. Being an endophyte, the majority of this mistletoe lives as a mycelial-like network of filaments that wrap around the vascular tissues of the host cactus. The only part of the mistletoe that ever emerges are the flowers. They come in both red and yellow forms. What may appear to be lovely cactus covered in red flowers are actually the flowers of Tristerix. Strangely enough, the occasional small leaf is produced on the flowering branches. Though there is chlorophyll in the leaf, researchers believe that they perform little if any photosynthesis.

Fruiting   Tristerix aphyllu s

Fruiting Tristerix aphyllus

This is not a parasitic relationship that is unique to cacti either. Africa has its own endoparasitic mistletoe as well. However, as we have discussed before, Africa does not have any native cacti (http://on.fb.me/1zPbac7). Instead, through convergent evolution, plants in the genus Euphorbia have followed similar adaptive trajectories. As such, at least one species of African mistletoe has followed suit.

Flowers of   Viscum minimum

Flowers of Viscum minimum

A species known scientifically as Viscum minimum finds the cactus-like Euphorbia horrida and E. polygona to its liking. Like Tristerix, Viscum minimum is endoparasitic, living entirely within the tissues of its Euphorbia host until it decides to flower. It too produces brightly colored berries that aid in its dispersal to a new host. 

The main seed dispersers are birds. After consumption, a bird either regurgitates the embryo or passes it out the other end. If that bird happens to be sitting on a host cactus or Euphorbia, the embryo will grow into a seedling that quickly taps into its new host and begins its internal parasitic life. It will not be seen again until it flowers.

Viscum minimum  beginning to set seed.

Viscum minimum beginning to set seed.

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


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