Japan

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Camel Crickets and the Dust Seeds of Parasitic Plants

A common way for plants to disperse their seeds is to entice animals to eat their seed-bearing fruits – a strategy known as endozoochory. Undigested seeds have the potential to travel long distances in the belly of an animal, and when they are finally deposited, a bit of fertilizer joins them. Discussions surrounding this method of seed dispersal usually have birds and mammals playing the starring roles – vertebrates, in other words. But what about invertebrates like insects? Do they have a role to play in transporting seeds within themselves?

Certain insects are absolutely important in the dispersal of seeds, particularly ants. But ants aren’t known to eat fruits and then poop out seeds. Instead they carry seeds to new locations, and some of these seeds go on to grow into new plants. In certain cases there is an elaisome attached to the seed, which is a nutritious treat that ants are particularly interested in eating. Elaisomes or arils have also been known to attract other insects like wasps and crickets, which may then become agents of seed dispersal. But endozoochory in insects, at first, seems unlikely. How would seeds survive not being crushed by an insect’s mandibles or otherwise destroyed in the digestion process?

camel crickets eating fruits of parasitic plants (via New Phytologist)

While observing parasitic plants in Japan, Kenji Suetsugu wanted to know how their seeds were dispersed. Many parasitic plants rely on wind dispersal, thus their seeds are minuscule, dust-like, and often winged. However, the seeds of the plants Suetsugu was observing, while tiny, were housed in fleshy fruits that don’t split open when ripe (i.e. indehiscent). This isn’t particularly unusual as other species of parasitic plants are known to have similar fruits, and Suetsugu was aware of studies that found rodents to be potential seed disperers for one species, birds to be dispersers of another, and even one instance of beetle endozoochory in a parasitic plant with fleshy, indehiscent fruit. With this in mind, he set out to identify the seed dispersers in his study.

Suetsugu observed three achlorophyllous, holoparisitic plants – Yoania amagiensis, Monotropastrum humile, and Phacellanthus tubiflorus. While their lifestyles are similar, they are not at all closely related and represent three different families (Orchidaceae,  Ericaceae, and Orobanchaceae respectively). All of these plants grow very low to the ground in deep shade below the canopy of trees. Air movement is at a minimum at their level, so seed dispersal by wind is not likely to be very effective. Using remote cameras, Suetsugu captured dozens of hours of footage and found camel crickets and ground beetles to be the main consumers of the fruits, with camel crickets being “the most voracious of the invertebrates.” This lead to the next question – did the feces of the fruit-eating camel crickets and ground beetles contain viable seeds?

Monotropastrum humile via wikimedia commons

After collecting a number of fecal pellets from the insects, Suetsugu determined that the seeds of all three species were “not robust enough to withstand mastication by the mandibles of the ground beetles.” On the other hand, the seeds passed through the camel crickets unscathed. A seed viability test confirmed that they were viable. Camel crickets were dispersing intact seeds of all three parasitic plants via their poop. The minuscule size of the seeds as well as their tough seed coat (compared to wind dispersed seeds of similar species) allowed for safe passage through the digestive system of this common ground insect.

In a later study, Suetsugu observed another mycoheterotrophic orchid, Yoania japonica, and also found camel crickets to be a common consumer of its fleshy, indehiscent fruits. Viable seeds were again found in the insect’s frass and were observed germinating in their natural habitat. Seutsugu noted that all of the fruits in his studies consumed by camel crickets are white or translucent, easily accessible to ground dwelling insects, and give off a fermented scent to which insects like camel crickets are known to be attracted. Camel crickets also spend their time foraging in areas suitable for the growth of these plants. All of this suggests co-evolutionary adaptations that have led to camel cricket-mediated seed dispersal.

Yoania japonica via wikimedia commons

Insect endozoochory may be an uncommon phenomenon, but perhaps it’s not as rare as we once presumed. As mentioned above, an instance of endozoochory by a beetle has been reported, as has one by a species of cockroach. Certainly the most well known example involves the wetas of New Zealand, which are large, flightless insects in the same order as grasshoppers and crickets and sometimes referred to as “invertebrate mice.” New Zealand lacks native ground-dwelling mammals, and wetas appear to have taken on the seed dispersal role that such mammals often play.

Where seeds are small enough and seed coats tough enough, insects have the potential to be agents of seed dispersal via ingestion. Further investigation will reveal additional instances where this is the case. Of course, effective seed dispersal means seeds must ultimately find themselves in locations suitable for germination in numbers that maintain healthy populations, which for the dust seeds of parasitic plants is quite specific since they require a host organism to root into. Thus, effective seed dispersal in these scenarios is also worth a more detailed look.

Further Reading:

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For more stories of seed dispersal check out the first issue of my new zine, Dispersal Stories.

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Biodiversity Dips When Japanese Rice Paddies Go Fallow

Large-scale farms that generally grow a single crop at a time and are managed conventionally are, by design, lacking in biodiversity. Abandoning such farms and allowing nature to take its course should, not surprisingly, result in a dramatic uptick in biodiversity. Plant colonization of abandoned farmland (also referred to as old field succession) is well studied and is regularly used as an example of secondary succession in ecology textbooks. The scenario seems obvious: cease agriculture operations, relinquish the land back to nature, and given enough time it will be transformed into a thriving natural community replete with diverse forms of plants and animals. This is an oversimplification, of course, and results will vary with each abandoned piece of land depending on the circumstances, but it generally seems to be the story. So what about when it isn’t?

Rice farming in Japan began at least 2400 years ago. Rice had been domesticated in China long before that, and when it eventually arrived in Japan it shaped the culture dramatically. For hundreds of years rice was farmed in small, terraced paddies in the mountains of Japan. Dennis Normile writes about these traditional, rice paddies in a recent issue of Science. He describes how they were found in villages “nestled in a forested valley” accompanied by vegetable plots, orchards, and pasture. Today, farms like these are “endangered,” and as they have become increasingly abandoned, plants, insects, and other wildlife that have historically thrived there are suffering.

Since the 1960’s, a combination of factors has resulted in the decline of traditional rice farming in Japan. For one, large scale farming has led to the consolidation of paddies, which are farmed more intensively. Diets in Japan have also shifted, resulting in a preference for bread and pasta over rice. Additionally, Japan’s population is shrinking, and residents of rural areas are migrating to cities. Traditional rice farmers are aging, and younger generations are showing little interest in pursuing this career.

Red rice paddy in Japan - photo credit: wikimedia commons

Red rice paddy in Japan – photo credit: wikimedia commons

Demographic and dietary concerns aside, why in this case is the abandonment of agriculture imperiling species? The answer appears to be in both the way that the rice paddies have been historically managed and the length of time that they have been managed that way. Agriculture, by its very nature, creates novel ecosystems, and if the practice continues long enough, surrounding flora and fauna could theoretically coevolve along with the practice. When the practice is discontinued, species that have come to rely on it become threatened.

Traditional rice paddies are, as Normile describes, “rimmed by banks so that they can be flooded and drained.” Farmers “encouraged wild grassland plants to grow on the banks because the roots stabilize the soil.” The banks are mowed at least twice a year, which helps keep woody shrubs and trees from establishing on the banks. In some areas, rice farming began where primitive people of Japan were burning frequently to encourage grassland habitat. Maintaining grassland species around rice paddies perpetuated the grassland habitat engineered by primitive cultures.

As rice paddies are abandoned and the surrounding grasslands are no longer maintained, invasive species like kudzu and a North American species of goldenrod have been moving in and dominating the landscape resulting in the decline of native plants and insects. Normile reports that the abandoned grasslands are not expected to return to native forests either since “surrounding forests…are a shadow of their old selves.”

Additionally, like most other parts of the world, Japan has lost much of its natural wetland habitat to development. Rice paddies provide habitat for wetland bird species. On paddies that have been abandoned or consolidated, researchers are finding fewer wetland bird species compared to paddies that are managed traditionally.

The gray-faced buzzard (Butastur indicus) is listed as vulnerable in Japan. It nests in forests and preys on insects, frogs, and other animals found in grasslands and rice paddies. It's decline has been linked to the abandonment and development of traditionally farmed rice paddies. (photo credit: wikimedia commons)

The gray-faced buzzard (Butastur indicus) is listed as vulnerable in Japan. It nests in forests and preys on insects, frogs, and other animals found in grasslands and rice paddies. Its decline has been linked to the abandonment and development of traditionally farmed rice paddies. (photo credit: wikimedia commons)

All of this adds fodder to an ongoing debate: “whether allowing farmland to revert to nature is a boon to biodiversity or actually harms it.” Where agriculture is a relatively new practice or where conventional practices dominate, abandoning agriculture would be expected to preserve and promote biodiversity. However, where certain agricultural practices have persisted for millenia, abandoning agriculture or converting  to modern day practices could result in endangerment and even extinction of some species. In the latter case, “rewilding” would require thoughtful consideration.

The thing that fascinates me the most about this report is just how intertwined humans are in the ecology of this planet. In many ways humans have done great harm to our environment and to the myriad other species that share it. We are a force to be reckoned with. Yet, the popular view that we are separate, above, apart, or even dominant over nature is an absurd one. For someone who cares deeply about the environment, this view has too often been accompanied by a sort of self-flagellation, cursing myself and my species for what we have done and continue to do to our home planet. Stories like this, however, offer an alternative perspective.

Humans are components of the natural world. We evolved just like every other living thing here, and so our actions as well as the actions of other species have helped shape the way the world looks. If our species had met its demise early in its evolutionary trajectory, the world would look very different. But we persisted, and as it turns out, despite the destruction we have caused and the species we have eliminated, we have simultaneously played a role in the evolution and persistence of many other species as well. We must learn to tread lightly – for the sake of our own species as well as others – but we should also quit considering ourselves “other than” nature, and we should stop beating ourselves up for our collective “mistakes.” It seems that when we come to recognize how connected we are to nature we will have greater motivation to protect it.

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The Discovery of a Living Fossil

In the early 1940’s, the genus Metasequoia was only known scientifically in fossil form. It had, in its day, been a widespread genus, found commonly in many areas across the Northern Hemisphere. It thrived among the dinosaurs. However, sometime during the Pliocene, the genus was thought to have died out. Thousands of fossils were left behind, and that would have been the end of the story had a member of its genus not been discovered still alive in a Chinese province later that decade. Its discovery is easily one of the greatest botanical stories of the 20th century, fascinating in its own right. The circumstances surrounding its scientific description, as it turns out, are equally interesting.

In the January 2016 issue of Landscape Architecture Magazine, Kyna Rubin details the event in an article entitled The Metasequoia Mystery. It’s the type of story that you almost need a crazy wall to sort out. A broad cast of characters interacted at various levels in order to make this profound discovery during a tumultuous time when the world was at war and China was being invaded by Japan.

Speaking of Japan, let’s start there. In 1941, Japanese paleobotanist, Shigeru Miki, published research describing fossils that for decades were thought to be either Sequoia or Taxodium as a new genus, Metasequoia. As Rubin points out, due to the war, “not every Chinese botanist would have had access to recent international research, let alone articles by botanists of an enemy country.” This could explain why in 1943 when Zhan Wang – a professer of forestry at Beijing University and the forest administrator for the Ministry of Agriculture and Forestry – was introduced to a living Metasequoia by an old classmate and local villagers in the Hubei Province, he wasn’t sure what he was looking at.

The tree was obviously important to the local people. They called it shuisa (water fir) and had built a shrine around it. Wang collected several branches and some cones that had fallen on a rooftop. At the time he identified it as Glyptostrobus pensilis (water pine), a tree common to the area; but he may have wondered if this was correct.

Eventually Wang’s samples and the details of his collection were brought to the attention of Wanjun Zheng, a dendrologist at the National Central University. Intrigued, Zheng sent his graduate student, Jiru Xue, to collect more samples from the same tree that Wang had encountered. These samples were more complete, and when they were presented to Xiansu Hu – the director of Fan Memorial Institute of Biology in Beijing – the mystery was solved. Hu had access to Miki’s research and concluded that what they had was a living fossil.

In 1948, Hu and Zheng published a paper describing the species and giving it the official name, Metasequoia glyptostroboides. The discovery ignited the botanical community as well as the general public, and soon seeds of what became commonly known as dawn redwood were being disseminated across the globe. Unfortunately, Wang’s contribution was not mentioned in the original paper, and the exact account of the discovery became convoluted.

photo credit: wikimedia commons

Dawn redwood (Metasequoia glytostroboides) is a deciduous, medium to large tree. Its cones are round and about 1 inch long. Its leaves are oppositely arranged and have a feather-like appearance. Its bark is fibrous, stringy, and red-brown to gray in color.  (photo credit: wikimedia commons)

At some point, a discussion between Zheng and a forester named Duo Gan (also known as Toh Kan) revealed that Gan had come across the tree in 1941, but he did not make any collections. Despite Zheng learning of Gan’s encounter after Zheng and Hu’s original paper had been published, Gan’s story became prominent, further obscuring the role that Wang played.

It’s important to note that none of Wang’s original collections were used as the type specimen – the particular specimen of an organism to which the scientific name is formally attached and is referred to in the scientific literature. The type specimen was collected by Xue. This is not uncommon, as initial collections may not always be in the best condition and may not include all the parts and pieces necessary to identify and describe a new species. But, as Rubin notes, “it was Wang’s specimens [that Zheng and others] had first examined and those specimens brought the tree to their attention to begin with.” So Wang’s contribution is an important part of the story.

Thanks to Wang’s former students, his role in the discovery has received greater exposure. Jinshuang Ma in particular has made it his mission to highlight the part that Wang played in the event. Apart from maintaining a website all about Metasequoia, Ma also spent several years searching for a lost herbarium specimen collected by Wang, which he found in an abandoned herbarium in Nanjing. You can read about his find in this article from the August 2003 issue of the journal Taxon. (Ma’s well researched summary of the events surrounding the Metasequoia discovery is also worth reading.)

Failure to acknowledge Wang’s contribution (at least initially) perhaps didn’t make waves outside of China, but in Rubin’s words, “the omission of Wang’s contribution sparked immediate hullabaloo inside China’s botanical circles in the late 1940’s.” Power and class differences likely played a big role. Hu and Zheng were established scholars that had received their educations in the United States and France respectively. Wang was young, from a remote village, and had not studied abroad. While Wang “went on to become one of China’s most distinguished forestry experts and botanists,” he was early in his career at the time of the Metasequoia discovery.

A deep respect for the elders in his field may be the reason that Wang’s students claim that he “never complained” about his treatment. His students go on to say that Wang “was not interested in personal gain,” and instead was simply satisfied to see that Metasequoia “was now growing successfully all over the world and was better protected.” It is listed as endangered on the IUCN Red List and would likely be extinct in its shrunken native range had awareness of its existence not come about when it did.

Fossil of Metasequoia occidentalis - photo credit: wikimedia commons

Fossil of Metasequoia occidentalis – photo credit: wikimedia commons

There are plenty of other interesting details to this story. Read the full article and check out the links on metasequoia.org to learn more. The account of Jiru Xue (also known as Hsueh Chi-Ju), the graduate student who collected the type specimens, is particularly interesting. Suprisingly, the tree Wang and Xue took their collections from is still alive today and is estimated to be over 400 years old.

Other longform article reviews on Awkward Botany:

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Hundreds of Japanese Plants Threatened with Extinction

Life has existed on earth for at least 3.5 billion years, and during that time there have been five mass extinctions. Currently, we are in the middle of a sixth one. The major difference between the current extinction event and others is that this one is largely human caused, which is pretty upsetting. However, knowing that detail has its upside: if humans are the drivers of this phenomenon, we can also be the ones to put on the brakes.

Biologists have spent the last several decades tracking the current mass extinction, endeavoring to come up with a list of species that have the greatest risks of extinction, as well as lists of species that are at less of a risk, etc. The problem is that factors leading up to extinctions are diverse, and available data for making predictions is lacking, especially temporal data. Recognizing this information gap, researchers in Japan set out to better determine the extinction risk of Japanese flora. Using data from surveys done by lay botanists in 1994-95 and 2003-04, they were able to calculate a trend which indicated that, under current circumstances, between 370 and 561 plant species in Japan will go extinct within the next 100 years.

photo credit: wikimedia commons

photo credit: wikimedia commons

The methods for this study, as described in the findings which appeared last month in PLOS ONE, involved dividing Japan into 3574 sections measuring around 100 square kilometers each and covering about 80% of the country. More than 500 lay botanists tallied the numbers of species that were found in each section during the two time periods. 1735 taxa were recorded, and out of those, 1618 were considered quantifiable and used in the analysis.

Japan is home to a recorded 7087 vascular plant taxa. Historically, the extinction rate of plant taxa in Japan has been around 0.01% per year. According to this study, over the next 100 years the extinction rate will rise to between 0.05 and 0.08% per year. Researchers are organizing a third census in the near future in order to monitor the actual extinction rate and better determine the accuracy of this prediction.

Data collected in these censuses was also used to evaluate the effectiveness of protected areas and determine the need for improvements and expansions. Natural parks cover 14.3% of Japan, but only about half of that area is regulated for biodiversity conservation. The researchers found that protected areas do help to reduce the risk of extinctions, but that their effectiveness is far from optimum and that even expanding protected areas to cover at least 17% of the nation (a target set at the recent Convention on Biological Diversity) would not effectively gaurd threatened plant species from extinction.

In their conclusion, the researchers advise not only to expand protected areas but to improve the “conservation effectiveness” of them, and “to improve the effectiveness of them, we need to know the types of pressures causing population decline in the areas.” They go on to list a few of these pressures, including land development and recreational overuse, and suggest that management schemes should be developed to focus on specific pressures.

Japanese Primrose, Primula japonica (photo credit: eol.org)

Japanese Primrose, Primula japonica (photo credit: eol.org)

One thing I found very interesting and encouraging about this study was the recruitment of lay botanists in collecting data. As stated in the findings, “Monitoring data collected by the public can play an essential role in assessing biodiversity.” I am excited by the growing citizen science movement and hope to see it continue to expand as more and more people become interested in science and eager to add to this body of knowledge. In fact, I consider the term “awkward botany” to be synonymous with citizen, lay, and amateur botany. That is precisely why I chose it as the title for my blog. So, in short, expect more posts involving citizen science in the future.

You can read more about this study on John Platt’s blog Extinction Countdown at Scientific American.