Art by Sun-Hyuk Kim
April 21st, 2023
What about our experience as fleshy, thumb-bearing, humans, can be shared with a resilient patch of daisies or a sturdy, hardened, oak? Quite a lot, when you consider that we are all formed of the same materials and shaped by time and natural selection to perform the interrelated tasks of growth, survival, and reproduction. For our green friends, various adaptations coined 'plant functional traits' have been accrued, modified, and lost throughout their consistent and biosphere-shaping reign on our planet to address these primary objectives. After a brief introduction on the background of functional trait research, we'll delve below the surface to focus more closely on root functional traits, why they are important, and how they shape ecosystems. It's not a far stretch to see how our own specie's adaptations, powered by our thumbs and tools, allow us to adjust and simultaneously redesign environments across the globe, just like those belonging to our autotrophic planet-mates.
Viewing Plants Through Trait-tinted Glasses
Before we get our hands dirty investigating belowground root traits, it would be beneficial to define plant functional traits and why some scientists have adopted a trait-based approach to ecology. Here's how ecologist Sandra Díaz defines the subject in question, “Functional traits are morphological, biochemical, physiological, structural, phenological, or behavioral characteristics that are expressed in phenotypes of individual organisms and are considered relevant to the response of such organisms to the environment and/or their effects on ecosystem properties.” I'll provide a simplified and ineffective explanation for any of you readers out there who aren't feeling Dr. Díaz's wonderful but wordy description - a plant functional trait is any measurable characteristic that impacts how a plant approaches the whole "life" thing. Are you a live-fast and die-young kinda plant, sucking up all life has to offer in the here and now. Or are you a conservative, invest in your tissues and 401k kinda plant, with long-term plans and dreams? While you ponder that philosophical enquiry, let's look at how all this talk about traits entered the plant science conversation.
Over a century ago, researchers began connecting quantitative measures of plant growth to specific leaf characteristics. One of these characteristics, or traits, if you will, would become known as specific leaf area (SLA). SLA is the ratio of leaf area to leaf dry mass, and because a larger leaf area can capture more sunlight (and therefore produce more sugars to build more tissues), it can serve as an accurate indicator of a plant's life-strategies regarding its rates and efficiencies of nutrient acquisition and growth. As the story all too often seems to go, this discovery led to plentitudes of aboveground research while inadvertently ignoring the universe below our feet. Nevertheless, leaf traits were the initiating ripple in the waters of ecological research that soon amounted to a trait-based wave of studies that shaped how we understand plant ecophysiology, biogeography, and evolutionary history today. Full disclosure: the bitterness displayed here is all a part of my online persona, and at my core I appreciate leaves just as much as roots, but what can I say - the drama really ups the blog's user engagement.
As we now know, SLA was a big hit, and everybody was super excited about leaves and what they can tell us about plant strategies and blah blah blah. All of this foliage frenzy led to the development of the leaf economics spectrum (LES) in the late 90's, and while I was busy choreographing performances with my Spice Girls figurines in the bathtub, scientists Peter Reich, Ian Wright, and many more, were preoccupied with less urgent matters such as investigating the relationship between leaf nitrogen content, life-span, photosynthesis, respiration rates, and SLA. A worldwide analysis was organized in hopes of determining if plants fell along a global spectrum of fast (acquisitive) to slow (conservative) nutrient return on biomass investment, and ever-so-conveniently for me and the hard-hitting science journalism I'm doing at this very moment, they found evidence for such a spectrum. Further disclosure: I spent way too much time thinking about a pun that would utilize the title of a Spice Girls hit song and end this paragraph with a bang. Just imagine a world in which I pulled it off, and it was really clever, and you laughed a lot ... and it spiced up your life.
Morphological: anything involving form and structure. This not only includes an organism's external structures, but also internal shapes and configurations.
Phenotype: the observable characteristics of an organism that are driven by both genetic makeup and the environment. Genes are providing organisms with a set of traits, and the environment(s) the organism develops in will tweak some of those traits. Basically, "genotype + environment = phenotype." The below diagram provides an example of how a phenotypic trait like plant height can be impacted by elevation.
Specific leaf area (SLA): the area of a single leaf, or all leaves in a tree's canopy, divided by the dry mass of said leaf/leaves. The inverse of SLA, leaf mass per area (LMA) is also used by scientists, depending on what questions they're asking. If focusing on growth rates, SLA is the usual go-to. When focusing on leaf longevity and the investments plants make in proteins per unit of leaf area, LMA is preferred.
Leaf economics spectrum (LES): A theory describing the aboveground trade-off in plants between resource acquisition and leaf construction costs. This trade-off can be observed in the relationships between traits such as LMA, leaf respiration rates, and leaf nitrogen and phosphorous content.
The empirical evidence supporting the LES led to further studies on other plant traits such as wood density and crown architecture, and it was shown that traits are linked within species and individuals (e.g., a plant with a fast leaf strategy will also exhibit high rates of water conduction using a fast wood strategy), and all biomes house plant communities consisting of species that exist along this 'fast-slow' gradient of nutrient acquisition and growth/life-span. If I lost ya there, I'll provide you with an example of how this impacts both individual plants and entire ecosystems. Let me introduce you to our two tree guests, the quick weeping willow and the sluggish Japanese maple. The willow, equipped with a high quantity of cheaply constructed leaves, captures tons of sunlight and uses large diameter vessels to pump the water needed to support fast photosynthetic rates and respiration. As a result of all this hurried work, the willow is rewarded with a large sum of photosynthates which are then used to support plant growth. On the other end of the spectrum, the Japanese maple invests a lot of time and carbohydrates into the construction of its tissues. Its leaves are thicker, capturing less light, and its vessels are smaller in diameter but higher in quantity. These traits lead to slower nutrient acquisition, but longer life-span, and in many cases, higher resistance to stress.
As I mentioned earlier, ecosystems are composed of a wide variety of fast and slow species, so how do these traits factor into forest dynamics and competition? Fast tree species will have high max growth rates and a low tolerance for competition during their seedling years. In times of resource excess, the willow will most likely out-compete the neighboring Japanese maple. However, when resources are scarce, the maple will be able to hunker down with minimal amounts of stress, as the willow freaks out like a guy with low blood sugar in a Snicker's commercial. You can see how both fast and slow traits are optimal under different conditions, and most systems operate at their own unique equilibrium of fast/slow species depending on factors like successional stage, biome type, disturbance, and more. In understanding these traits on an individual, species, and community level, we can begin to grasp whole-ecosystem responses to biotic and abiotic factors, such as invasive species and climate change. If you remain confused as to what plant functional traits are or why they are important, I recommend checking out this presentation by Dr. Reich before we traverse underground and get rooty.
Fine-root Functional Traits
Hey! Since you're on youtube already, fully immersed in my recent recommendation, why don't you make it a viewing party and watch Dr. Luke McCormack's presentation on linking root traits to ecosystem processes. That would save me the hassle of defining what class of roots we're talking about here. Plus, as per our official contract (which Luke has signed and is definitely not something I just conjured up for amusing blog material), I will receive a yearly supply of rare Chinese teas per every thumbs up on this five-year-old video. It's never too late to go viral.
Contractual obligations aside, because there's no way for me to know if you, the reader, watch anything I have ever suggested throughout the history of this blog, I will briefly summarize the first section of Luke's talk. When we're thinking about belowground functional traits, and therefore tree water and nutrient acquisition, we have to look at a specific class of roots called fine roots. Unlike the large coarse roots that serve anchorage and storage functions for trees, fine roots are positioned on the most distal end of a tree's root system and are generally grouped as anything >2mm. Plot twist: because root diameter varies vastly amongst tree species, the >2mm cut-off isn't always sufficient in targeting absorptive roots, and when it's possible, it would be better for researchers to use an order based system that is more likely to select the fine roots responsible for absorptive functions rather than transport functions. Below you'll find an image from a 2015 publication by McCormack et al. that will hopefully aid in your absorption of this message.
Order based system of fine-root classification: borrowed from scientists who've studied the natural branching patterns of rivers and streams, this method of classification labels the most distal roots within a system as 1st orders.
Absorptive fine roots:
the lowest order of fine roots within a root system, responsible for acquiring soil nutrients and water.
Transport fine roots: higher order roots that result from the merging of multiple absorptive roots, responsible for transporting nutrients and water through the root system.
Okay, now we know what class of roots we're looking at, but why venture below the topsoil at all? If we know that plants land somewhere along a 'fast-slow' spectrum, and that the functional traits driving their rates of nutrient acquisition and growth line up across organs, why not just assume a tree with fast aboveground strategies is as equally fast belowground? Depending on the root scientist you ask this question, you may receive different answers, but here I will defer to Dr. Monique Weemstra and co's 2016 paper because I think they offer succinct explanations for this inquiry (and whose illustration can be seen here).
Let's begin by admitting the obvious: roots are much more complex, dynamic, and mysterious, compared to their aboveground counterparts because of the diverse multitude of biotic and abiotic pressures they face within the soil, the numerous functions they perform, and the mycorrhizal interactions that make this whole belowground story more tangled. Soil texture and chemistry influence fine-root growth and exploration, and in addition, roots must acquire water and 15 essential nutrients from different soil types. Some root traits may enhance uptake of a specific nutrient, while impeding another, and you can see how this muddies our understanding of root functions when aiming to link them to measurable traits. The sophistication doesn't end there, as interactions with mycorrhizal fungi also influence root traits and functions. For instance, a fine root may thicken and slow down its metabolism (i.e., slow traits) in order to provide the best home for a fungal tenant to move in, but that mycorrhizal fungi could then increase that root's nutrient uptake (i.e., fast trait). Because of this complicated belowground landscape and the various adaptations roots have evolved to coexist there, a simple spectrum comparable to the LES is not applicable to roots.
By now, I'm sure I've thoroughly convinced you that roots are a beautiful, labrinythian, disaster of a research focus that everyone should dedicate their lives to, but to satisfy the rest of the human population who seems to be so obsessed with things they can see during their afternoon walk, we can aim to address how root traits impact the aboveground world. Just like the broader category of plant functional traits covered at the start of this trait tale, root functional traits influence not only individual plants, but whole-ecosystem community structure and nutrient cycling. For us curious folk who enjoy learning for the sake of blogging or annoying their friends with information they didn't ask for, root traits can give us insight into fun topics like species biogeography, evolutionary history, and ecosystem interactions. For the more applied-minded tribe, root traits can assist us in identifying plants that can tolerate certain environments and stressors such as water and nutrient abundance or limitation. Last but not least, for all of you perplexing peeps who enjoy modeling as a past-time, root traits have significant impacts on ecosystem net primary productivity and carbon cycling.
Hopefully I've been successful in my attempts to unearth the messages that root functional traits require a more complex spectrum than the acquisitive - conservative model typically used in aboveground ecology, and that the consideration of these traits is important when aiming to understand whole-ecosystem dynamics. Exciting research over the last 15 years has deepened our knowledge of the evolutionary forces fine-tuning fine-roots, root trait impacts on plant nutrient and water relations, and the multibranched interactions that all of these belowground traits have on one another. Before I get into the current literature, I'll give you some actual traits to hold in your conceptual root trait repertoire.
Imagine a scenario where I've dragged you to a social function populated by hundreds of renowned root traits who are all standing around, mingling, and I've been granted the marvelous opportunity of introducing you to each of them. Instead of pawning you off on Mrs. Root-calcium-content after exclaiming that you both enjoy dairy products, maybe it's best to dig in where we left off aboveground. Earlier I explained the discovery of SLA and how this leaf functional trait led to an understanding in plant investment versus return of resources in the form of sunlight capture and subsequent photosynthate production. The closest belowground equivalent would be specific root length (SRL), which is essentially telling a similar story where resource acquisition (root length) is divided by resource investment (root dry mass). Root diameter (RD) is another important phylogenetically conserved root trait studied frequently because of its relation to SRL, nutrient foraging strategies, mycorrhizal fungi colonization, and simply because it's convenient to measure. To throw more traits at you (because you seem really adept at small talk and the root traits just adore you), there's root tissue density (RTD), root nitrogen content, root respiration, root branching intensity, root branching ratio, and over 300+ more if you want to visit the Root Trait Inventory over at Oak Ridge National Laboratory's website.
Resources such as the Fine Root Ecology Database, cutely acronymized as 'FRED' and linked above, have worked to pool root data from all over the world and provide researches with information on hundreds of root traits spanning across a diverse range of species and biomes. To the distinguished root traits you met earlier, this is their home - The Hamptons for root traits, if you will. If you happened to take an interest in any of the traits previously mentioned, which for some odd reason I've decided to personify as affluent East Coasters (what does this say about me), you can zero in on that specific trait using the helpful categories listed on the trait inventory page: "root anatomy, architecture, chemistry, dynamics, morphology, physiology, whole-root system, and microbial associations." If you're looking for a more detailed understanding of these traits, as well as their connections to one another, you can check out this 2017 paper by McCormack and colleagues which offers a lot of cool rooty material, such as the image of EM fungi and their root hosts shown below.
Specific root length (SRL): I may have defined SRL multiple times on this blog by now, so for those of you rolling your eyes at my redundancy, I apologize ... for being thorough and thoughtful! Okay, so SRL is the belowground analogue to SLA that compares acquisition potential to tissue investment. One of the first scientists to use SRL when looking at root functions and ecosystem processes was Alastair H. Fitter, who also happened to be the scientist responsible for applying the order-based system to roots. Dr. Fitter, if you see this, visit the root lab sometime. We would all enjoy picking your ear about the underground, and also, I'm eager to meet someone with the name 'Alastair.'
Phylogenetically conserved: genes, and therefore traits, that are retained through a specie's evolutionary history with few to minor changes. Examples include the proteins cytochrome c and hemoglobin that can be found in mammals and all other organisms that depend on oxygen for respiration. These proteins serve such vital functions that any mutation acquired is typically selected against and not reproduced. This is evolution's way of communicating "if it ain't broke, don't fix it!"
Root diameter (RD): the measurement of length across the body of a root.
Root tissue density (RTD): the ratio of root dry mass to root volume. The story of this trait starts to get pretty complicated when considering the different tissue layers within a root. For example, the cortical tissue layers in the middle of the root are less dense than the inner stele tissue.
Root nitrogen content: the mass of nitrogen per root mass. I think it is fair to say that this particular trait has caused quite the headache for some researchers, as it doesn't "behave" the same way, or tell us the same things, as leaf nitrogen content. What we do know is that it is largely driven by soil traits and nutrient availability, and impacts root litter decomposition rates as well. Fine roots with higher nitrogen content and lower carbon content decompose at faster rates.
Root respiration: the amount of CO2 released from a given mass of roots. Roots with higher respiration rates are "breathing" or "working" harder, just like you may find yourself doing after powering your way through this long blog post.
Root branching intensity: number of lower-order roots per centimeter length of higher-order root.
Root branching ratio: number of roots in a given order divided by the number of roots in the higher order.
Congratulations, you've thoroughly networked with all the traits at this made-up root gala, listening to them talk on and on about their root children, philanthropic ventures, and how much phosphorous they've absorbed this year. Let's now transport ourselves back in time to witness just how these traits have evolved. If you can recall from an earlier post that overviewed the adaptations plants refined while making their transition to land, the Cretaceous (145-65 mya) was a prolific period for plant diversification and geographical expansion into different habitats. It was like the Renaissance for trees, and you should take that simile very seriously coming from someone who knows extremely little about the historical relevance of the Renaissance and slightly more, but still not that much, about plant evolution. Anyway, poets nor trees can escape the influence of the geologic time of their existence, and both end up being shaped by their environment while simultaneously impacting it. This 2012 publication by Comas et al. does a fantastic job explaining just that - the connection between the evolutionary forces of the Cretaceous environment, the resulting tree adaptations, and the subsequent shift in Earth's biogeochemical cycles.
All of the above images are showcasing the most ancient woody roots from lycopods that existed during the Carboniferous, which occurred between 360-300 mya (much earlier than the Cretaceous, but still a great example of how roots have evolved over time). These fossils are called stigmaria, which is a type of 'form genera,' meaning that they are grouped based on a part of the organism rather than by species. Geologists use this classification system because organisms such as large trees tend to fossilize specific parts (e.g., leaves, cones, and bark) that are found spatially separate from one another. Shout out to the geology department at Kentucky University who provided me with these pictures, and make sure to check out that link if you're interested in learning more about stigmaria - UK does a great job at explaining the specifics of the stigmaria fossilization process.
The above paper, as well as the later 2018 research conducted by Ma et al., emphasizes the importance of RD, SRL, and mycorrhizal fungi association types as three traits that show distinct changes over evolutionary timescales, high phylogenetic signals, and significant influences over nutrient uptake strategies and other interrelated root traits. As atmospheric CO2 decreased during the Cretaceous, and leaves increased their stomatal conductance and leaf vein density to maintain photosynthetic rates, roots had to increase their efficiency belowground to support these aboveground adaptations. Simultaneously, decreased CO2 caused slower decomposition rates in soils, limiting the pool of mobile soil nutrients, and we begin to see the origins of the first ectomycorrhizal fungi evolving separately in different lineages of trees. It is because of these circumstances that tree species across the globe have generally evolved lower RD, higher SRL, and less dependence on arbuscular mycorrhizal fungi over time.
These trends towards lower RD and higher SRL reduced the energy costs of root production, increased water conductance and nutrient uptake rates, and extended the available root surface area for ectomycorrhizal colonization. Species descending from more ancient lineages tell a different story. This can be seen in roots within the Magnoliaceae family, which exhibit thicker RD compared to more recently evolved tree species. Though magnolias are primitive flowering plants that have many unique characteristics, I'm mentioning their root-based differences here to provide support for the strong phylogenetic influence on some morphological root traits. For those of you who missed the definition of 'phylogenetically conserved' amongst the extremely important and fun to read vocabulary words defined above, this means that a specific region of DNA has remained mostly unchanged in many groups of related species. These segments of DNA are highly heritable, consistent, and code for genes that serve vital functions. This is all to say that the persistent evolutionary direction of fine roots seems to be leaning towards thin and nimble, but, a tree's ancestral history still has some say in the manner.
A diagram I'm borrowing from the previously mentioned Comas paper that's showing root diameter (in millimeters) of 20 tropical and subtropical angiosperm trees. I found this extremely helpful when trying to visualize how recently evolved species trend towards lower RD.
Trait Interactions with Water and Nutrients
Now that we've reviewed a brief background check on the evolutionary and phylogenetic histories of these three root traits, I'll quickly address how RD, SRL, and mycorrhizal fungi association impact water absorption and nutrient uptake. The enhancement in soil exploration strategies that a low RD and high SRL offer directly impact the access to available water and nutrients. Thin and soft roots are able to weave their way through small soil pores like nubby contortionists, and being bendy really comes in handy when in competition with other organisms or in seasonal/infertile environments where water and nutrients are sporadic. The ability of a plant's root system to quickly proliferate new growth in response to abiotic (e.g., rain and temperature) and biotic cues (e.g., herbivory and soil microbe interactions) are also linked to RD and SRL, again with lower RD and higher SRL species performing better in this area. Researches would label a plant wielding these root traits and the accompanying soil exploration strategies as a fast/acquisitive species, but we know from our tree tale at the beginning of this post that the speedy willow doesn't always win the race.
Associations with mycorhizzal fungi also influence access and uptake rates of water and nutrients. Increases in EM fungal colonization in particular greatly expand a tree's ability to explore the soil via hyphal networks, and such networks have longer life-spans than the more ephemeral AM built structures. In addition, mycorrhizal fungi participate in the formation of different 'nutrient economies' because of their impact on soil nutrient availability through decomposition. Fungi within the AM group are primarily assisting trees with phosphorus uptake. They also pass along nitrogen, which they uptake from pools of inorganic N. Their more versatile counterparts, EM fungi, are able to access organic N pools, as well as weather minerals, to offer a more diverse nutrient payment to their tree hosts. These differences are driven by each group's inventory of enzymes. The later-diverged EM fungi have evolved stronger saprotrophic capabilities (or rather, never lost them) which allows them to access organic forms of nutrients through decomposition in a manner that is not available to the AM group. Both fungal groups play a pivotal role in not only individual plant nutrient uptake, but also nutrient cycling in forests and plant and soil community structure. Despite my urge to dive deeper into this subject matter, I will stop right now, thank you very much (Spice Girls lyrics), and encourage you to take a look at the paper I linked earlier in this paragraph, which is co-authored by Morton's very own Dr. Meghan Midgley, and is also the source of the informative graphic below.
Exploring the Connections Between Traits
There are innumerable examples of how these traits of interest inevitably end up influencing other root traits, and if I really wanted to show you my quirky hyper-fixation side, I would take over a wall in the lab and connect all 300+ root traits using newspaper clippings and strings of red yarn. For now we'll limit our focus to the impacts on root lifespan, root branching intensity, and root branching ratio. Root lifespan is positively linked to root diameter, and therefore negatively to SRL. Roots with higher diameters are investing more in tissue construction, leading to higher root longevity. This has been linked to other plant traits such as root calcium content and plant growth rate. McCormack et al. found that temperate trees with thicker roots had up to a three-fold increase in root lifespan. The exact mechanism driving this increase has yet to be fully uncovered, and it is my suspicion that thicker roots have access to an expensive anti-aging cream which they apply nightly. In actuality, explanations involving root anatomy likely influence this trait (e.g., a thick exodermis could support higher root lifespans because it prevents desiccation, herbivory, and offers a stronger barrier to plant pathogens). Kong and co. explored this further, but more research is needed to elucidate the relationships between root lifespan and other root traits.
The complicated story involving mycorrhizal colonization and root lifespan is a little more fuzzy and requires additional exploration before making any definitive statements on how these two traits interact. In AM species, mycorrhizal colonization has been shown to increase root lifespan by enhancing tolerance to drying soils and protecting against root pathogens, but these results are dependent on the tree and fungal species involved, as well as the available resources (e.g., water, nitrogen, phosphorous, etc.). For instance, Hooker and colleagues found Populus roots colonized by AM fungi to have shorter lifespans. Studies on EM fungal colonization and root lifespan are even more sparse, but I did find an interesting study by Liese et al. reporting on a dried soil experiment. The results showed fine roots colonized by EM fungi to have shorter lifespans than those with AM fungal partners by ~50 days when in drought conditions.
Root architectural traits such as root branching intensity and branching ratio show strong relationships to mycorrhizal colonization type and weaker associations to the phylogenetic signals that influence RD and SRL. We can turn to another publication by Liese and colleagues for evidence supporting this claim. Architectural trait relations with mycorrhizal fungi show observable trends in angiosperm AM and EM species, with EM species generally showing higher root branching intensity that allows them to produce highly clustered root growth and exploit nutrient rich patches in the soils. Contrastingly, AM species show low root branching intensity, and rely more on changes in root morphological traits (specifically RD) to coordinate with their fungal partners for nutrient acquisition. These strategies can look a little different for gymnosperm EM species, who show low branching intensity due to the even distribution of sparse nutrients in the soils they are typically found growing in. Multiple studies have shown architectural traits to be less constrained by species lineage and more plastic than morphological traits such as RD, SRL, and RTD. This suggests that root branching intensity and branching ratio allows plants to adapt to a variety of environmental and nutrient conditions.
The Race to Uncover a Multidimensional Root Trait Spectrum ... that works
The second Liese paper linked above provides us with a smooth segue to the end of this section, as the group also found correlations between root architectural traits and aboveground traits, which implies that some root traits may serve as increasingly accurate indicators of fast and slow species. This is not only important for figuring out a root economics spectrum (RES) that makes sense, but also for tying these traits and processes to the aboveground economy. To offer a rudimentary summarization of Liese's findings, intensive root branching leads to low C:N ratios and high SRL in fine roots (i.e., fast traits), which indirectly causes high SLA and short leaf longevity (also fast traits). Below is a diagram from the Liese et al. paper that may further confuse you or make this more digestible. Let me know in my non-existent suggestions box, or better yet, allow your virtual voices to be heard in the comment section on Luke's youtube lecture.
If my explanations of the frequently measured root traits above have painted a clear picture for you regarding a universally agreed upon RES, then you should start questioning that picture now. In the last decade alone, there has been a lot of research showing the inconsistencies of linking root traits to strategies, functions, and to each other. This is especially true when looking at morphological traits such as RD, SRL, and RTD. To return to the Weemstra paper linked earlier in this post, issues pinning down an RES that is analogous to the aboveground LES arise because of the complex functions root must perform, the multitude of environmental factors roots they face, as well as the diversity in type and function of their symbioses with soil microbiota. This has led to continuous tweaking of the axes on the root economic spectrum, as well as many unanswered questions.
So, where are we at now? Should we bury all hopes for a cohesive RES and call it a day? Recent research by Bergmann (2020) and Yi (2023) suggests not, and through summarizing their findings maybe I can glue all of this together into somewhat of a cohesive narrative and finally set you free from this virtual entrapment. By pulling from global trait measurements of close to 2,000 species (woody and non-woody), Bergmann and colleagues were able to find evidence supporting the addition of a mycorrhizal collaboration axis to the classic conservation axis. This collaboration gradient was driven by SRL, RD, and cortex fraction, with thin rooted species (i.e., high SRL) relying on their own roots for water and nutrient acquisition, and thick rooted species (i.e., high RD and cortical space) investing in larger roots that can be colonized by more mycorrhizal fungi, therefore outsourcing their uptake needs. The diagram below depicts Bergmann's framework in addition to the classic fast-slow spectrum driven by root nitrogen and root tissue density.
Yi and colleagues added to the complexity of the above model by emphasizing the role of root function in the RES. Researchers have been stressing the importance of measuring functional/physiological traits in addition to the frequently measured morphological ones, but as I've mentioned many times in this blog, studying roots is challenge. This is especially true when trying to measure ongoing processes like root respiration, exudation, and so on. This paper focused on measuring root nitrogen uptake rates, and found that high SRL was not associated with higher nitrogen uptake, which differs from the conventional view that a fast trait like SRL will have higher nutrient uptake rates. This finding led the authors to incorporate an 'amount-efficiency' spectrum driven by trait morphology and physiology. In addition, they found higher branching ratios caused higher mycorrhizal fungi colonization rates, therefore a 'self-symbiosis' axis was driven by root architectural traits. These discoveries aren't replacing the former model that rests on the relationship between RD and AM mycorrhizal fungi colonization rates, but rather adding to it. Imagine a model where axes of low to high branching ratio and RD run parallel alongside low to high mycorrhizal fungi colonization rates. If you can't imagine it, I don't have an image for you, and I would suggest that you work on your child-like wonder.
Although we've reached the end of this trait tour, much like the Spice Girls, I'm not finished performing! Now that you all have been introduced to plant and root functional traits and their importance, when returning to this subject we'll take a look at how climate, soil, season, and plant functional types influence global root trait variation. There's also a lot of ground to cover regarding mycorrhizal fungi's influence in the belowground space, and I'll be sure to dig into that as well.
Art by Utagawa Hiroshige
Listen to the tree
February 22nd, 2023
For this next post, I thought I would resist drowning you all with any further waterlogging related info, and instead take in a metaphorical breath of fresh air with some unrelated root and tree topics. Let's all put on our best berets and art-critiquing-faces as we take a peek at the creative endeavors of both the Root Lab volunteers and ancient to modern Asian civilizations. First up, we have some epoxied pieces of fine art that provide informative 3D glimpses of fine roots, followed by an historical account of the art of bonsai.
Over the last couple of weeks, our Root Lab volunteers have been staying busy during the quiet and cold winter season by epoxying fine root samples. Epoxy resin is commonly used to encase specimens of plants, animals, minerals, and more. Thanks to the patient and creative work of Jen, Larry, and Don, we have a diverse catalog of fine roots to share.
From start to finish: Don and Larry can be seen here, first cleaning the roots and then placing them in the epoxy moulds.
Not only are these branching beauties fun to look at, they also show us important morphological and functional differences between the fine roots of different species. Researchers often study root traits such as root diameter, specific root length, root architecture, and the relationship between root tissue density and mycorrhizal fungi colonization. Tune in to the next blog post to learn more about the above. In the meantime, see if you can spot some of the species' variation below.
The history of bonsai
From the earliest complex human societies in China, nature has shaped Eastern culture like water slowly carving rivers in the terrestrial terrain. One of the oldest examples of this shaping is the practice of mimicking natural landscapes by miniaturizing trees and other potted plants. Archeologists continue to debate the exact initiation of these customs, but some suggest it became a cultural norm as far back as 4,000 years ago. More conservative estimations date the preembryonic stages of bonsai closer to the 1st century C.E., as a ritual carried out by Daoist mystics. Whatever the pre-calendar calendar year, the distillation of the ineffable beauty and vastness of natural sites into miniature forms was ritualized as an act of appreciating the energy and forces that sculpt the world around us. As an added bonus, these mini shrines could be brought into the home, garden, and other sacred spaces for people to maintain their connection to nature, regardless of any physical separation that became increasingly apparent as societies continued to develop.
As goes the story of all developing nations, immigration and outside cultural influences eventually clash or meld with preexisting ways of life. The introduction of Indian Buddhism in the 2nd century C.E., and the later sect of Chán Buddhism that would result from Indian and early Chinese philosophies blending together, just so happened to perfectly compliment traditional indigenous practices. Harmony with nature, a core Daoist teaching, paired nicely with the meditative practices of Buddhism and both religions also had their own traditions of potting plants and miniaturizing landscapes. By the time we see written documentation of primitive forms of bonsai during the Tang dynasty in 700 C.E., the art was far from the beginner's level that you'll find in your local Home Depot today. More evidence of the advanced craft was found in Prince Zhang Huai's tomb mural in 706 C.E., which showed miniaturized fruit trees planted in trays with pebble soil mixtures.
This tray-based landscape design, then called penzai, would continue to develop in China and split off into different categories. Another translation, penjing, meaning 'potted landscape/scenery,' is the term you'll find widely used today. This includes tree penjing, shumu, that implements the tools of wiring and pruning to shape trees, landscape penjing, shanshui, which carefully places rocks and water to recreate natural scenery, and shuian penjing which combines the elements of the first two in addition to other small figurines for finer detail of the landscape. Penjing continued to evolve and disperse throughout Asia, eventually hitching a ride on Chán Buddhism across the East Sea to Japan.
An ikadabuki raft style penjing landscape by Matyie Che followed by a map showing the spread of Buddhism throughout Asia.
Around the 6th century, as the first Buddhist students were returning to mainland Japan with miniaturized tree souvenirs in tow, specific clans and noble classes were adopting Buddhist thought and rituals throughout the islands. The Soga clan, consisting mostly of Korean immigrants, were influential in the initial acceptance and adoption of these principles. Buddhism would receive official government support as a state religion in 587 C.E.. As I mentioned previously, external influences sometimes clash with a nation's preexisting culture, and Buddhism wasn't entirely embraced by all of Japan's citizens. The widely practiced indigenous religion, Shinto, had rooted itself in Japanese culture since 300 B.C.E., and it wasn't necessarily clear how these two philosophies would coexist moving forward.
After a series of minor battles, Buddhism and the Sogas came out on top. As Buddhism became more widely practiced, the middle and lower societal classes of Japan were gently encouraged to accept the status-quo. Many Shinto beliefs were assimilated into the Chán school of Buddhism, resulting in Japanese Zen Buddhism. Shinto, with its emphasis on the intrinsic energy and power in nature and all living beings (that intrinsic energy being kami), complimented the meditative and introspective philosophies of Buddhism. These principles would soon be reflected in the arts of the time.
The first Japanese literary references to miniaturized trees can be found around the year 1000 C.E., and 300 years later, scroll artists began illustrating dwarfed trees in tray landscapes as accessory elements and main subjects of their work. The oldest of the latter can be admired in Kasuga-gongen-genki, a masterpiece consisting of 20 painted scrolls, detailing the miracles carried out by Buddhist and Shinto deities of the Kasuga shrine and temple located in the Nara prefecture of Japan. The beauty in austerity was a continuous thread weaving together this era's religion, philosophy, and art. What better way to exemplify this notion than to engage in a relationship with a living tree by meticulously shaping and training its form as it responds with an inherent drive to grow?
The Edo period (1603-1868) and the Meiji Restoration that followed also led to important developments within the practice, popularization, and cultural significant of bonsai. The political stability of the Edo period allowed for a lively art scene. Potted trees, along with many other nature-inspired art forms (woodblock prints, scrolls, sculptures, ceramics, textiles, and screen paintings), quickly grew in popularity within urban centers like beds of moss enveloping a lusterless stump. By the time Emperor Meiji came around and dissolved Japan's feudal system, restoring imperialism and initiating the movement of the country towards its modern era, bonsai was a main focus of many Japanese nurseries located in cities such as Kyoto and Osaka. As Japan opened itself up to trade and foreign travel, bonsai were shipped to Europe and North America. Meanwhile, accounts from travelers such as Marie Stopes and Robert Fortune provided insight into Japanese aesthetic and the miniaturized trees that could be found in most wealthy households and businesses. This led to international interest, which spurred bonsai-related publications and exhibitions in cities world-wide.
This Buddhist statue in Japan was built in 609 C.E. and depicts the Great Buddha of Asuka-dera. The following image shows one of the 20 scrolls that comprise the Kasuga-gongen-genki. In the left section of the painting you can see bonsai and saikei propped up on work benches.
Migration to the West
Earlier we covered the Chinese art of penjing and you may be wondering why the western migration of miniaturized trees was rooted, instead, in Japanese culture. Was there no influence from China, Vietnam, or other East Asian countries that have their own history of potted landscapes? The answer to this question is complex and undoubtedly related to many of the rifts that exist between East- and Western cultures. To provide somewhat of a simplified explanation, it has a lot to do with the different barriers to assimilation that U.S. Japanese and Chinese immigrants experienced in the mid to late 1800's.
The California gold rush in the 1850's, and the need for laborers in the newly admitted Hawaiian state, resulted in a high flux of Chinese and Japanese immigrants over the course of a couple decades. The first generation of Chinese immigrants in California consisted of mainly young males who were treated poorly both by the communities that surrounded them and the mining industry in which they were employed. Assimilation was not easy for this demographic, and issues were only exacerbated by the 1883 Chinese Exclusion Act passed by the U.S. government. Over the next 60 years, the Chinese population would dwindle until the 1942 Magnuson Act repealed the immigration ban. During the years of the Exclusion, Chinese-Americans established Chinatowns in San Francisco, New York City, Boston, Philadelphia, and Chicago, but due to racial biases, Chinese culture wouldn't be appreciated by the general population until much later.
Much like the highly prized bonsai that made their way to the Hawaiian islands during the late 1800's, the Japanese-American immigration story is one that begins with embracement. From 1850-1900, the Japanese population in Hawaii sky-rocketed as the islands were in need of a skilled workforce. At the turn of the century, many Issei (a term meaning 'first generation') immigrated to the contiguous states and became farmers. Japanese-Americans would soon have a strong influence in the horticultural field, especially around the West Coast. Ornamental nurseries were established, and the art of bonsai began percolating through American culture.
These circumstances differed from the Chinese-American experience described above for a number of reasons. First off, and perhaps most importantly, it seems that Issei were more respected and accepted by their fellow American citizens, but this is something I can only infer from historical accounts, and I'm sure the dynamics were much more nuanced than what can be gleaned from wikipedia. Also, most of these men were trained in traditional arts and crafts, and it was easier for them to practice and eventually spread important traditions surrounding art, food, and general ways of life. Furthermore, many of them were able to return to Japan, marry, and bring their families back to the states. All of the above aided in the establishment of Japanese-American communities and the embracement of their traditions into Western culture.
Hopefully we all have a clear understanding of why and how bonsai was transferred to us in the West via Japan rather than any other East Asian influence, otherwise my attempts at impersonating a virtual middle-school history teacher were unsuccessful. I don't know if you caught my foreshadowing up there, but Japanese-Americans would come to face their own discriminatory treatment, as the U.S. halted immigration in 1924 and later established war relocation centers in 1942, forcing over 120,000 Japanese-American citizens and immigrants to abandon their homes, businesses, and bonsai. We will return to this later, as it is an important historical period that shaped the lives of many, as well as the legacy of bonsai.
43-year-old juniper presented in a cascade style at the Hawaii Bonsai Culture Center.
Statue of Japanese sugarcane workers in Kepaniwai Heritage Gardens, Maui, Hawaii.
88-year-old crepe myrtle in an informal upright style at the Hawaii Bonsai Culture Center.
Beginning in the 1890's, high quantities of miniaturized trees were being exported from Japan to the U.S. and Europe. During the next 30-year period, exotic plant species were crossing continental borders in frequencies that would never again be matched. This was a time before plant importation and quarantine laws, so there was less worry surrounding the spread of infectious plant diseases, and more worry about having a diverse selection of non-natives at your local nursery. The term bonsai was not used in English-language catalogs. Instead, Japanese nurseries would refer to miniaturized potted trees as trained, dwarfed, hachinoki (Japanese term for 'potted tree'), or naninized (Latin term for 'small'). The Hinoki cypress, or Chabo-hiba (Chamaecyparis obtusa), was the most popular specimen bought by European and American customers during this three-decade span. It was stylized into a distinct pom-pom shape, similar to what most people would visualize when hearing the word 'bonsai.' This species and style wasn't very popular in Japan, but it was easy to grow, inexpensive, and large, and therefore appealing to us fast-paced Westerners.
Just to re-emphasize, and probably over-romanticize, this marvelous time in horticultural history, the late 1800's not only saw the influx of new bonsai species, but also millions of other unfamiliar Japanese species and bulbs. This led to the establishment of gardens in parks, public spaces, and home landscapes. The first ever Japanese garden built and exhibited in the states took place during the 1876 Philadelphia Centennial Exposition. This was most likely also the historical debut of bonsai in the states. Two years later, Europeans at the Paris International Exhibition had their first encounters with bonsai at exhibits run by visiting Japanese nursery owners and artists. The first public presentation about bonsai and tree care was said to take place in Chicago at the World's Columbian Exposition in August of 1893. During this presentation, a Japanese nurseryman named Henry Izawa described the process of producing miniaturized trees and gardens. Slowly but surely, these public displays were planting seeds of interest and wonder in Westerner's hearts.
According to Charles Long's An Informal History of Bonsai, which served as an extremely informative source material for this post, there were multiple types of publications that initiated the establishment of bonsai in North America. These include nursery catalogs produced by Japanese nurseries for an English market, bonsai articles in English and French magazines, English books published in Japan for both foreigners working in Japan and for those focusing on how to grow the trade outside of country boundaries, and finally, books published in English in the U.S. and Europe. Prior to these accessible reads, there was a prolific boom of Japanese bonsai material that covered tree care practices as well as stylistic choices and the philosophy behind the art. Japanese-American's such as Bungo Miyazawa, Iwao Yoshimura, and Sawada Ushimaro all published popular books in the early 1900's, and Norio Kobayashi began publishing the innovative Bonsai Magazine in 1931. However, these works were inaccessible to English speaking audiences, and if you were a Westerner taking up bonsai prior to WWII, you were most likely learning by trial and error.
A nearly 300-year-old Hinoki cypress at the Arnold Arboretum. Check out the link for some interesting info on this specimen. Above you can also see some retro bonsai magz from the 70's. I was unable to find any of the original Kobayashi publishings from the 30's, but many of his books are still available online.
As we all know from the FX show The Americans, or Showtime's Homeland, spies are a SERIOUS THREAT TO NATIONAL SECURITY AND THEY MUST BE STOPPED. Just like our modern television networks, former President Franklin D. Roosevelt really cared about spies, and stopping them. Preventing espionage, in addition to worries over economic competition and the deep-rooted racism towards Asian groups in the western states, was a main justification for the Executive Order 9066. In 1942, after the attack on Pearl Harbor, FDR signed this policy, which circumvented any constitutional questionability by allowing the U.S. Army to set up military zones in locations that just so happened to be populated by Japanese communities. As a result, the first generation Issei described earlier, as well as second-generation Nisei who had citizenship by birthright, were forcibly removed from their homes within a 48-hour notice. Individuals and families were then relocated to one of ten internment camps further inland, where they would spend the next three or more years until the end of WWII.
My intention behind rehashing our country's history is not to condemn our past behavior, but rather to celebrate the resiliency of the Japanese population by discussing how they continued to connect and express themselves through the art of bonsai as they endured inhumane treatment. For FDR and many of our U.S. officials and citizens who could not find it within themselves to accept those who were culturally unfamiliar, their own fear of what they didn't understand led to destructive thoughts and actions. This is a pattern we see time and time again. Unfortunately, if you are human, you are liable to make the same mistakes in the name of what you feel is "good," or simply in following the status quo. Let's challenge ourselves to look for the space to be open-minded, compassionate, and curious people, even when our first instinct may be self-preservation.
Back to Order 9066 and what life looked like for the Japanese-American citizens and immigrants living in the internment camps during the 1940's. Living conditions were poor and cramped in the camps, without any trace of comfort from the familiarity of prisoners' past lives. To prove their loyalty to the U.S., many Japanese-Americans left behind traditional Japanese items, and whatever they did bring was limited by what they could carry. For professional nurserymen, this meant prioritizing trees over clothes and furniture. Skilled practice and tending to bonsai continued in the camps, as did many other traditional arts and crafts.
We can look at the lives of Frank Nagata and Morihei Furuya who trained under their teacher Sam Tameichi Doi at Camp Amache in Granada, Colorado, for an example of this continuation of traditional art and culture. All of these men influenced the bonsai scene in the western states prior to their relocation, and much of their collections had to be abandoned. Similar to how any logical parent would react to all of their children hanging off of a cliff, you save your favorites. Before you are offended by that comparison, I would like to defend myself and state that I think that is an apt comparison, long-time bonsai practitioners care deeply about their trees! Anyway, those lucky plants that made the cut, as well as whatever dwarfable trees were found on site, became the new locus of attention for Nagata, Furuya, and Doi. Just like their trees who miraculously survived the cold and bitter winters and the hot, dry, Colorado summers - these men endured the tribulations at Amache, only to grow in complexity in both their artistic skill and human spirit.
After WWII ended, bonsai and those practicing it had to reacclimate to a changed world. Property and possessions weren't returned. Businesses were lost. Between $2 to $5 billion worth of assets were lost. Individuals and families had to start from the ground up. Doi's students Frank Nagata and Morihei Furuya would do just that by joining three others in the founding of the Southern California Bonsai Society. This club would go on to popularize bonsai in the western states, building a large community that later transitioned to the California Bonsai Society.
A glimpse of life inside the camps. These pictures show a drone's-eye-view of camp Amache, children outside of their one-room school house, and the cramped living quarters that families had to endure. Head over the the Digital Public Library of America to see more pictures. You'll only find a few images inside the camps because photography wasn't permitted.
When considering individuals who's life work focused on spreading the art of bonsai to all those who were interested, beyond the stark boundaries that a language gap is prone to construct, teachers Haruo Kaneshiro, John Naka, and Yuji Yoshimura deserve recognition. Kaneshiro established a new inclusive branch of the Hawaii Bonsai Association in order to allow admittance to all, leading the world in the category of tropical bonsai. Naka and Yuji's catalogs and contributions each call for their own blog posts, but I will do my best to summarize their work here.
Raised in Japan and inspired by his grandfather and a love of nature, John Naka would later move to the U.S. and become the most renowned bonsai teacher in the Western scene. Rising in popularity due to his attractive teaching style, supplemented with proverbs and drawings/paintings that would help guide his students, Naka began to tour different states in the 1960's. His books Bonsai Techniques I (1973) and Bonsai Techniques II (1982) are staples in the bonsai community and have been translated in Spanish, German, French, and Italian. He's received various prestigious awards from Japan and the U.S., and continued to pursue his creative endeavors late into his 80's.
Yuji Yoshimura influenced the expansion of bonsai from over seas after a childhood of exposure to plants and bonsai and a degree from the Tokyo Horticultural school. After establishing his bonsai nursery in 1948, he began teaching classes and would go on to instruct over 600 students in the decade that followed. Being one of the founders of the Nippon Young Men's Bonsai Association (NBA), he played a large role in encouraging Western bonsai practitioners to visit Japan for training. Yoshimura, as well as Naka, also encouraged bonsai masters from the NBA to travel West to give lessons. This constant transference of both practical skill, tree care techniques, and creative styling, between the East and West was a key component in the proliferation of bonsai.
Two great examples of Yoshimura's collaborative approach and encouragement of others in the field include his work with Alfred Koehn and Giocanni Halford. Koehn was a writer and artist who helped to educate English-speaking students attending Yoshimura's classes in his Tokyo nursery. Halford was also a writer, who would later assist Yoshimura in writing The Japanese Art of Miniature Trees and Landscapes in 1957. This would become the standard training manual for those practicing bonsai in the West. I don't know if it reached the record sales of literary masterpieces like Twilight or one of the 37 Harry Potter books, but it was considered the "bonsai bible," so that has to account for something.
Although we are nearing the end of this historical stroll down hachinoki lane, the art and practice of bonsai is far from over. Thanks to the efforts of those mentioned above, and many others who I couldn't afford to squeeze in due to the fact that my readers surely have other important things to attend to (like their bonsai trees, or reading my other posts, or watching The Last of Us to prepare for a fungi induced pandemic), bonsai was firmly established in the West by the 1960's. In 1967, the American Bonsai Society was formed, and continues to be a great resource for state clubs, instructors, classes, and other learning opportunities.
John Naka in a wonderful hat. If you're looking for a place to see some of his more famous trees, as well as their stories, check out this pdf.
Women in bonsai
While reading the above chronicles of bonsai, you may have noticed the lack of representation of woman. This phenomena is not only observed in the world of miniaturized trees, but in most art forms, as women artists are both paid less for their work and granted less awards than their male counterparts. Maybe they just need to cut off an ear to be taken seriously. Anyway, I want to take a moment to acknowledge some talented bonsai professionals that weren't covered in the above bonsai briefing: Kathy Shaner, Marija Hajdic, Pauline Muth, Amy Liang, and Chicako Yamamoto. I have linked their websites and/or bonsai club profiles which provides a brief description of their work and accolades. Also, check out this blog post by Samantha Holm if you are interested in seeing some data on women in the arts and in bonsai. It's a great read!
Appreciating the art and the living medium
In researching the history of bonsai, and watching a not-obsessive-at-all-completely-normal amount of bonsai youtube videos, ideas regarding the difference between East- and Western thought slowly began to bloom in the bright and highly sophisticated corners of my mind. Hopefully we know each other well enough by now that you sense my facetiousness, I have absolutely no merit to be dolling out my opinions on subjects like art theory and philosophy, but I'm going to do it anyway because I am the ultimate authority here!
This comparative discussion written by Jeff Humphries describes the stark difference in a much more elegant manner than I ever could, but for those of you who don't feel like reading 25 pages of dense cultural criticism, the author focused heavily on the Westerner's relationship with nature. Humphries argues that because we see ourselves as separate from the forests, the trees, and most all living and non-living elements with which we share this Planet, our foundational understanding of our own existence is distorted. This is reflected in our art, our relationships with other animals, and even our approaches to conservation and environmentalism. This sentiment is echoed here by the previously mentioned Charles Long, "It is difficult to define the appeal of these demanding tree forms. Perhaps the one common denominator which explains the lure of bonsai is their expressiveness of freedom. As man sees himself crowded by burgeoning populations and a rapidly narrowing ratio of square footage per person, the bonsai becomes symbolic, as it did in another context for the Buddhists, of a long-abandoned, far distant better time when man was a natural phenomenon in and not above nature."