Bioluminescence.

One of the more intriguing (at least to me), and beautiful quirks about the evolution of life on this planet is the repeated development of bioluminescence across many different lineages. Bioluminescence is simply the ability of a living organism to produce light. If it’s alive and luminescing, boom, you’ve got an example of a complex chemical cascade that allows sacks of meat not so different from ourselves to light up like a goddamned Christmas tree. Essentially, what is happening with bioluminescence is a highly controlled chemical reaction that releases energy in the form of light emission. This can be done by the beastie itself, or by a symbiotic microorganism that has been acquired by a larger creature. It occurs in multiple kingdoms of life, in terrestrial and marine environments. If I so desired, I could ruminate tearfully on how all of Earth’s life is chemically derived from components forged in a star in a Saganesque exposition of cosmic perspective…and how in some small way, bioluminescence is the means by which stardust can light the darkness of the universe once again. But, heavy-hearted sighs and poetic attribution of consciousness to a mechanically elegant and indifferent universe are for another day, and if done in all seriousness, for another person.

The thing about bioluminescence is that often our understanding of it is limited to a few well-known examples, and without any sort of context, biological or otherwise, other than ‘that is pretty; I like it.’ And while yes, indeed, fireflies and deep-sea fish do have a magical and/or alien quality to them, there is a whole world of bioluminescing organisms that go unloved and underappreciated and denied all the badass reasons for and applications of their abilities. Bioluminescence has evolved many times, and therefore, each example tends to have its own unique story.

First, the most conventional and familiar case of bioluminescence for many folks; fireflies.

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Fireflies aren’t actually flies. They are beetles, specifically of the family Lampyridae. They range all over the world in warmer latitudes, and tend to inhabit wet, soggy, swampy fields and meadows, or damp wooded areas. Their larvae also produce light, and are often referred to as ‘glow worms.’ Fireflies, both as adults and larvae, produce light from the ends of their abdomens in a special organ in which a chemical reaction involving the enzyme luciferase, magnesium, ATP (major molecular carrier of energy in cells), oxygen, and a light-emitting compound known as luciferin occurs. Luciferase can only work on luciferin in the presence of the other listed compounds, and the eventual outcome of the reaction is a relatively bright emission of ‘cold light’. The color of this emitted light ranges between species (and some species don’t even light up at all), and can be between 510 and 670 nanometers, which means green to yellow to almost red. The actual function of this ability differs for larvae and adults. Larvae use their constant glowing to notify predators that their bodies are currently producing chemicals that make them taste bad, toxic, and often both. A hungry bird looking for an evening snack learns quickly that the attractively squooshy beacons in the meadow grass taste less like food and more like sadness. When puberty sets in for these sparkly grubs, the function, of course, becomes sexual. What once was effective for deterring getting eaten, now is co-opted later in life for attracting mates through fanciful courtship displays. It’s a bit like how when you’re four years old, dancing and singing and running around were decent ways to burn off excess energy, but later on, if you do these things effectively, there’s a good chance you’re going to make a lot of money and get laid. So, subtle nuances of natural and sexual selection have driven firefly bioluminescence, and all of it is based on an enigmatic enzymatic reaction contained within the body of a living creature. Consider that the next time you imprison this wonder of nature in an old jam jar.

While popular imagery of fireflies surrounds lovely meadow nightscapes, dotted with the flickering bright lights of fairy-like insects, all under the silky light of the full moon, there are multiple dimensions to the the firefly. And some of these dimensions are ironically quite ‘dark’, as fireflies, like any other creature, are continually under the relentless force of natural selection, and their angelically-glowing butts serve no refuge from the brutal realities of nature. For example, take a look at the following two fireflies:

and

They look very much alike, right? And while it would be tempting to say that they are members of the same species, this is not true. However, they are close relatives. The top firefly is of the genus Photinus and the bottom is Photuris. Photinus are among the most commonly seen fireflies in the U.S., and some species use highly synchronized flashing in courtship behavior. Photinus males search for conspecific females in the darkness by making use of their strobe-light asses and flashing signals in a specific pattern. If a female likes what she sees, she responds with her own, typically much more subdued and demure neon laser in what eventually becomes some sort of silent woodland rave. In one species, P. carolinus, this matter-of-fact response of ‘yes, please’ from a female will often result in a mad rush of males to her location (as many as two dozen), in which they aggressively flash, and try to mount and inseminate the female, as well as other eager males that stray too close and look a little too sexy. After the dazzling light show (and, undoubtedly, random eruptions of clouds of firefly ejaculate) dies down and the impromptu orgy subsides, the female flies away impregnated and twenty-some males fly away satisfied. Confused, but satisfied.

Whenever a phenomenon that causes great fun in nature develops, there is always something that turns up with the primary intention to exploit the hell out of it.

That second firefly from above, Photuris, is that day-ruiner. Photuris fireflies are predators…of other firefly species. Instead of using their light-making powers for good and for procuring sexy times, they’ve turned it into a weapon; a light of ill-intent. Along the way, Photuris turned to the dark side of the Force. Somewhere in their recent evolutionary history, these fireflies discarded their green power rings for, uh, orange? Red? Whatever.

Photuris females have evolved the crafty, deceptive behavior of mimicking the affirmative response of the aforementioned Photinus female. Photinus males signal, Photuris females flash back in a perfect imitation, and the males converge to get some nookie, and then this happens:

It is this om nom noming of hapless, horny firefly males that has given this particular genus of firefly the name ‘femme fatale’ fireflies. Photuris also goes after other small insects, but the females of the species have specialized in dining on the males of closely related species. To describe this phenomenon in familiar human terms and scenarios, imagine that an attractive woman at a bar, who has been getting hit on by some half-intoxicated jagaloon, leads him out of the building. But, instead of the two of them leaving together, it turns out she’s a gorilla in a human-suit, and she dines on his organs in the middle of the alleyway. That is essentially what is going on here for these fireflies.

There are multiple examples of bioluminescence occurring in arthropods (like with fireflies), but only one example of it happening in millipedes, those many-legged, peaceful herbivores. Luckily, this example genus, Motyxia, can be found right here in the U.S. (err, assuming most of the people reading this are American). And, if you live on the West Coast, you’re in an even larger bit of luck. The eight species of Motyxia, known as Sierra luminous millipedes, are found only in southern California; specifically in the southern Sierras, the Tehachapi Mountains, and the Santa Monica Mountains. They can be found in giant sequoia and oak forests, and like most members of the order of millipede to which they belong (Polydesmida), they are completely blind. During the day, they spend much of their time underneath loose soil and leaf litter on the forest floor, and they look like this:

But when night falls, they emerge from their hiding places and crawl around feeding on rotting vegetation in the typical millipede fashion. However, in the darkness, unlike all other millipedes…

…they look like glow sticks with legs.

Not much is known yet about how bioluminescence works in Motyxia. It is only the exoskeleton that emits light, and it increases with intensity when the millipede is handled and/or agitated. Because if I could light up, and folks were bothering me about it, I’d try to crank up the power and blind them with my resplendence too. Scientists aren’t sure of the precise compound or reaction responsible for this, but it is known to be based on an unknown photoprotein, which tend to fluoresce when exposed to an outside factor (like UV light, such as in green fluorescent protein, or GFP). As for the evolutionary function, we aren’t too sure of that yet either. It would seem that such a property would be a bit of hindrance to survival in a forest full of hungry predators. Being a slow, blind, easily seen animal initially makes one think that these millipedes are suicidal, and are glowing on purpose. Some field studies have suggested that the bioluminescence acts as a warning signal to predators, as bioluminescence was shown to negatively impact predation rates. This strategy, similar to the role of bioluminescence in firefly young, would make sense, seeing as how like many species within the order Polydesmida, Motyxia produces cyanide in its body, making it one hell of an ‘impactful’ meal for a nocturnal shrew or fox.

For those of us living in the Pacific Northwest, we are likely already familiar with a close relative of Motyxia. In the same family (Xystodesmidae), is the yellow-spotted millipede, or Harpaphe haydeniana, and it can be found all along the northern Pacific Coast; from Alaska down to California.

These little guys are hard to miss. When I lived on the southern Oregon Coast, I’d see tons of them all over the place on the forest floor during the torrential and long-lasting winter rains. I’d curiously watch them walk over downed doug-fir branches and chunks of bark. At times I was tempted to pick them up and have them walk over my hands and forearms; I’m glad I never did this. Like the Sierra luminous millipedes, H. haydeniana can produce cyanide. It does this in the form of hydrogen cyanide (HCN), which is excreted through its exoskeleton when it is threatened. Of course, being picked up by inquisitive primates like ourselves very much counts as threatening behavior. It is because of this ability to squirt cyanide compounds through its exoskeletal joints that it is also called the ‘almond-scented millipede’, as cyanide can often smell like burnt almonds to humans that carry the allele for that particular genetic sensitivity to the odor. As a side note, if you are near a place that is storing or using hazardous chemicals, and the faint scent of almonds drifts along to you on a breeze, it would be wise to get your ass out of the area immediately.

Another lesser known bioluminescent animal is a terrestrial snail, Quantula striata, found in parts of Southeast Asia. It is the only known bioluminescent land gastropod (gastropod referring to Gastropoda, the group of mollusks containing ‘stomach footed’ animals like slugs, snails, nudibranchs, etc.).

There is little else unique about this humble animal other than the fact that its eggs will fluoresce slightly in the dark, and juveniles and adult snails can flash yellow-green light from a bioluminescent organ near the mouth called the ‘organ of Haneda’, named after the biologist who discovered the ability, Dr. Yata Haneda. The world of snail biology is obviously a frenetic and rapidly changing field, but the discovery of tan snails in tropical Asia with glowing faces in 1942 was likely upending enough to even throw the brakes on this endlessly tumultuous sub-discipline. The actual reason for this capacity in Q. striata is not yet known. It was once hypothesized that the flashing functioned as a means for juveniles to more easily find short-lived, perishable sources of food. By seeing their hatch-mates more easily in the dark forest understory surrounding a foodstuff, they could easily track down transient sources of food and have a better chance of survival; young snails would act as their own beacons for finding temporary sources of sustenance. However, little evidence exists for this hypothesis as of yet. An alternative function postulated by the world’s 6-year-olds is that flashing mouths make it easier for the snails to kiss in the dark.

While many bioluminescent organisms are of the creepy-crawly, distantly related variety, there are a large number of good ol’ familiar, spine-having vertebrates that have their own lights to turn on. All of these are fish, and most of them live in dark environments like the deep sea or subterranean cave ecosystems. Images of deep-sea fish have been popularized in recent decades, and most folks are well-acquainted with conventional examples like lantern fish, with their out-sized, glossy eyes, black bodies, and rows of pale, button-like light organs along their flanks. Also familiar to most are the anglerfish; grotesque, droplet-shaped monsters with loose skin, gaping maws, and a well-positioned shining lure; females carrying along a parasitic male, fused to her body and reduced to nothing but reproductive organs, hanging on like a mindless tumor, a withered hunk of scrotal tissue. The alien visages have been recreated in cartoonish and widely-accessible platforms, like Spongebob Squarepants and Finding Nemo, and thus the horrible (and yet, physically quite small) demons of the abyss have bled into our popular culture a minute amount. And while the ‘syndromes’ of traits common to deep-sea bioluminescent fish (large mouths and teeth, reduced bodies and fins, little pigmentation, large or absent eyes, strange body forms, eerie blue light producing organs, etc.) are widespread, there are two unique examples that need addressing.

When most people think of sharks, their minds immediately go to large, dynamic super-predators. Great whites. Hammerheads. Makos. Tiger sharks. Giant, sleek macropredators that rip into surfboards (and surfers) like Ritz crackers, and ravenously turn Captain Quint into a scarlet-colored ‘person salad.’ The reality is that while these keystone, charismatic species are certainly more visible and memorable, there are a lot of sharks that don’t fit the stereotype at all. One group are the dogfish, which make up the shark order Squaliformes. They tend to be small (smaller than a human at least), and not quite the pelagic death-torpedoes expected of the shark lineage. One particular kind of squaliform shark that is dramatically different from all other sharks is the genus Isistius, of which there are three species. They are known occasionally as ‘cigar sharks’ based on their chunky, elongated and comparatively un-athletic looking bodies.

Isistius really is somewhat of the stereotypical ‘nerd’ of the shark realm. Small, goggle eyed, with a receding chin and bulbous snout, and an ever-present collar. But, it is how Isistius earns its other, more widely-known common name, that gives this big-eyed, somehow adorable little shark a uniquely horrific place in the deep ocean. It is also known as the ‘cookiecutter shark.’

This name comes from how this shark goes about feeding itself. Cookiecutter sharks are the only parasitic sharks, and they target large fish and sea mammals. After intercepting prey, they fasten their highly-specialized mouths (equipped with a pair of suction-creating ‘lips’) onto the flanks of something like a marlin, a whale, or a larger shark. With the help of spiracles (or as non-biologists call them, ‘holes’) on the back of their head, it creates a tight seal on the surface. It closes the spiracles, and retracts its tongue, and the negative pressure makes it nearly immovable. After becoming a living Garfield suction-cup car window decoration, it bites down and digs into its victim with these babies…

The cookiecutter shark gouges into the hide of the unfortunate host with those insanely large lower teeth (which are so derived that they act as a whole unit, and are replaced as a row all at once, instead of individually like in other sharks), wheels in a circle, and then dislodges with a round plug of delicious flesh. It then moves on to another spot on the animal, or to another animal entirely. This feeding habit typically won’t kill the miserable soul subjected to being carved at like a plane of dough for making festive holiday baked goods, but it can weaken the animal to the point of it succumbing to secondary afflictions. Apparently, being covered in crater-like wounds takes a toll on the immune system. The scars associated with these sharks are ubiquitous on large sea mammals, and some dolphins will have entire holes missing from dorsal fins.

Humans aren’t immune from these feisty critters, and there have reports of attacks on underwater photographers, as well as capsized ship survivors, based on their descriptions of being bit in small, clean chunks as they floated along the waves at nighttime. The shark also routinely damages oceanographic equipment and underwater telecommunications cables. Even U.S. submarines have had to make changes from neoprene and rubber coverings on external equipment to fiberglass ones after cookiecutter sharks wreaked havoc on them, thinking they were a gastronomic jackpot.

So, observant reader, you are probably asking; what the hell does this have to do with bioluminescence? Cookiecutter sharks use photophores (small light producing organs that  appear as single, bright dots of light) to lure in a potential host in their dark, mesopelagic zone (the zone just deep enough for light to fail to penetrate) home. Almost the entire body is covered in these photophores:

However, cookiecutter sharks have a dark band of skin forming a collar near the head that does not light up. It is thought that the absence of bioluminescence in this one spot is the source of the lure. The hypothesis is that when the shark is producing light in all areas surrounding that collar, from the point of view of an animal below looking up at the bottom of the cookiecutter, the dark band looks like the silhouette of a small fish against the lighter surface waters way up in the water column. The shark would just slowly hang out and drift, suspended in the water column, its bioluminescence breaking up its figure from a deeper viewpoint by matching the downwelling light in a strategy known as counterillumination. The host would fail to see the outline of the cookiecutter shark looking up at the lighter waters above, and would instead see a vaguely fish-shaped, dark band. All that would be needed would be a close approach, and the cookiecutter shark would dine like a king.

The hellspawn pictured above is known as Malacosteus, or the ‘stoplight loosejaw’, and while that sounds uncomfortably like an antiquated euphemism for a prostitute you’d hear from your grandmother, it’s actually a deep-sea, bioluminescing fish. What makes the stoplight loosejaw unique is the way in which it uses its bioluminescence to catch prey. Most deep-sea animals that are bioluminescent produce green or blue light. Because longer and lower energy wavelengths of light (the reds and oranges and yellows) can’t penetrate into the ocean water that deep, most animals at these extreme depths aren’t sensitive to such wavelengths and subsequent colors. Instead, they can see higher energy  wavelengths like green and blue, which is appropriately the wavelengths they use to see and lure prey, as well as find each other for reproduction. The stoplight loosejaw has exploited this selective sensitivity to wavelengths of light through use of a separate, large photophore positioned right underneath the eye (observable below as a pale, banana-shaped patch):

This special photophore puts out a red light. Combined with a small, nearby green-glowing photophore, this arrangement inspired the fish’s common name. Stoplight loosejaws, it is thought, use large red light-producing photophores to illuminate the location of prey items without being seen by red-insensitive organisms. You see, the stoplight loosejaw also has the uncanny ability to see the red light it is producing; a trait very uncommon to deep-sea fish. This brilliant strategy of ‘I-see-you-but-it’s-physically-impossible-for-you-to-see-me’ is made possible through a certain component of the stoplight loosejaw’s diet. While it has evolved to eat moderately-sized fish as an ambush predator, it snacks between meals on copepods, which are small, plentiful crustaceans. From these copepods, it obtains a derivative of chlorophyll as a photosensitizer, which it then uses in its bizarre visual system. This derivative absorbs red wavelengths of light (at around 700 nanometers), and then stimulates two intrinsic visual pigments already present in the eyes of the fish, which have a maximum absorbances in the green-blue range (typical of most deep-sea fish). So, a molecular tool stolen from the stoplight loosejaw’s diet is used to bypass limitations set-up by millions of years of evolution of the deep-sea visual system, and allow for the recognition of red wavelengths. This system is a bit like eating a hamburger that allowed you to see through people’s clothes.

Bioluminescence is not limited to just mobile animals, and other kingdoms of life have gotten on the glow train. Fungi, denizens of our weird, moisture-loving sister kingdom, also have bioluminescent representatives. One of the most striking is Panellus stipticus, the ‘bitter oyster’ or ‘luminescent panellus’, found in deciduous woodlands over much of the Northern Hemisphere and Australia. It is an important ‘white rot’ (referring to the ability to break down lignin as well as cellulose and hemicellulose in wood, giving the rotting remains a soft, pale, mushy quality) fungus of hardwood trees, and most strains of the fungus produce some sort of greenish light in the majority of tissues in a mystical, Pandora-esque evening show.

Bioluminescent fungi like this (and there are some 60 known, diverse species) were the inspiration for the notion of ‘foxfire’, which dates back to at least Aristotle’s earliest account of the phenomenon some 2300 years ago. Foxfire, not to be confused with a similarly named internet browser, was simply a whimsical acknowledgement of strange glowing wood in the forest and in outdoor wooden structures. For centuries, foxfire was spun into supernatural yarns and included in the greater, pre-Industrial forest dweller mythos alongside such folklore as the Will-o’-the-wisp. It wasn’t until the 1820s that someone finally figured out the fungal origins and put all the superstitious nonsense to rest by examining a rotting support beam in a mine that housed a glowing fungus. Go Enlightenment!

We now know that bioluminescence in fungi is normally due to the luciferase reaction; the same chemical cascade seen in fireflies. As for its function, this is not clear. It appears over a wide diversity of distantly related fungal species, and appears to have evolved separately multiple times. Some have thought that it serves as a mechanism to attract insects or herbivores so that it can deposit its spores on their bodies, and have their genetic material dispersed throughout the forest. However, seeing as how in many species, the fruiting body (the ‘mushroom’ you actually see above ground) that contains the spores will not glow, while the subterranean mycelium network will luminesce…this hypothesis doesn’t seem like an adequate explanation.

If you’re thinking to yourself that eating one of these crazy neon caps will punch you a ticket to the psychedelic land of the Na’vi, please know that you will be sorely disappointed. While bioluminescent fungi give the impression of being saturated with mystical, consciousness-expanding powers, this impression really is only gills deep. Many bioluminescent fungi, while they appear as though they taste of sour apple and can transport you a neverending field of wonder and bliss, are actually quite cruelly toxic. One example is the jack ‘o lantern mushroom (Omphalotus olearius) of the northeastern U.S. It gives off a weak green glow in the dark, and looks like this:

Its similar appearance in the day time to chanterelles, and overall pleasing smell, makes poisoning by jack ‘o lantern mushroom relatively common. The effects are of the typical bad shroom variety; vomiting, stomach cramps, and explosive diarrhea until you wish for death. However, since the toxin in this species (illudin) is non-lethal, you’ll have to suffer through it for a few days. Lucky you.

So, remember kids, just because it looks pretty and smells pretty and looks a bit like something that is actually safe to eat…doesn’t mean you have the green light (so to speak) to make a meal out of it. I’m considering beginning a solo (oh and how could it be any other way) campaign to bring warning and skepticism to the realm of bioluminescent mushrooms. Of course, I’d have to combat shameless, irresponsible glorification of these fallaciously friendly fungi by the media and entertainment industry…

Up until now, I’ve only been talking about organisms that generate their own light via chemical processes in their own cells. There exists an entirely different route for bioluminescence to occur; stealing it from microorganisms. One such useful microorganism is Vibrio fischeri, which is found in our oceans. V. fischeri uses the familiar luciferin-luciferase pathway to generate light, and in its natural state, is a free-swimming organism. However, multiple multicellular animals have evolved a symbiotic relationship with the bacteria, and inoculate specialized organs with them, and house a regulated colony within themselves in order to cash in on the benefits of bioluminescence, while providing the bacteria with shelter and nutrition. One such relationship exists between V. fischeri and bobtail squid of the cephalopod order Sepiolida. Bobtail squid are closely related to cuttlefish and frequent shallow tropical waters of the Indian and Pacific Oceans. Their generally chunky, rounded mantles, short tentacles, and overall sickening levels of ‘kawaii-ness’ have also given them the names ‘dumpling squid’ and, I shit you not, ‘stubby squid.’ Bobtail squid have a light organ in their mantle which houses the bioluminescent bacteria, which they supply dutifully with hard-earned sugars and amino acids. In return, the bobtail squid can use the bacterial light to break up its silhouette against the downwelling sunlight or moonlight from above (much like with the cookiecutter shark), effectively camouflaging it from both prey and predator. The squid does this by careful articulations of the interior of the light organ, reflecting the light in tightly orchestrated ways between reflective surfaces. This alliance is effective for the survival of both partners, but there are still imperfections.

So yes, even tiny microorganisms routinely develop the capacity to engage in the great bioluminescence game. In fact, one of the most spectacular displays of bioluminescence comes from lowly single-celled organisms, once amassed in large numbers. The following example is dear to my heart, so I will undoubtedly come off as incredibly biased (but only because it’s the coolest thing I’ve ever seen).

These little fellows are Noctiluca scintillans, a common marine dinoflagellate protist found worldwide in shallow coastal waters. It is bound to these coastal regions because its chief food are photosynthetic algaes that require access to sunlight in shallow seas and continental shelves. They are capable of producing a blue-green light via small ‘microsource’ organelles that utilize the luciferin-luciferase system; literally thousands of these organelles pepper the inside of these lily-pad shaped cells. Individually, the light output from a single Noctiluca is negligible, of course. However, when conditions are perfect for the production of their food source (usually the result of seasonal circulation patterns merging with temporary high-nutrient conditions close to shore, increasingly due to nitrate pollution), a ‘bloom’ or ‘red tide’ occurs, and the density of microorganisms in the waves offshore explodes, including Noctiluca. What results is a ‘phosphorescent tide’, in which the waves literally glow an icy blue-green as they crash onto the shore. As the dinoflagellates are disturbed by mechanical motion of the waves, or by human swimming, they fire their lights, causing an impossibly beautiful seascape to unfold.

It is because of this effect during blooms that N. scintillans is often referred to as sea sparkle. I had the privilege of seeing this once when I lived on the Oregon Coast one warm summer night as a teenager. I was completely ignorant of the cause of this miraculous happening, and was caught up in the surprise and wonder of it all. Everything glowed brilliantly. When one stepped on the soaked sand as the most recent wave pulled away, the pressure from the foot would result in a radiating surge of glittery blue light to spread outwards across the sand, signaling the locations of stranded clumps of sea sparkle. Running through those cold waves that night, bathing in their transient, magical light, is an experience I cannot forget, and I hope to have once again.

So, bioluminescence is a bit of a recurrent ability in many forms of life on Earth. It’s used to get other members of the species in the sack, to serve as a clever trick to nab some grub, and to warn bigger and badder creatures to refrain from giving you a taste. It goes beyond the scope of a few select animals like fireflies and weird, abyssal fish, and fits into a broad range of evolutionary contexts. As seemingly special and otherworldly as bioluminescence is, in reality, it’s no more than another tool available to organisms on this planet to propagate their genetic material. Perceived beauty cannot detract from nature’s inherent indifference, no matter how much art or poetry we attempt to assign to it. Perhaps in knowing this indifference, that these gorgeous lifeforms illuminating the dark have no intent to awe us, to inspire us, makes them all the more beautiful. Their artfulness is accidental, as it should be, and we humans are observers, standing at the center of nothing, and certainly not their universe. Us and them? Just little bits of leftover stardust, glowing and non-glowing, drifting along like we have for billions of years. I’m not sure about you, but I’m pretty much okay with that.

*Tsuneaki Hiramatsu

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