Tag Archives: Buds

Tree Architectural Models

Halle & Olderman in the 1970s created a model of 23 types of architectural models to which all tree species are believed to conform. They started with the idea that the shoot apical meristem/s (“SAM” – the primary growing tip) is/are the ‘treemakers’.^ref The behaviour of the SAM over time determines the form of the tree. They identified four types of meristems (active growing shoots) which led to different forms – those with a single meristem (like a palm), those with modular construction which follow a precisely repeating pattern, trees with trunk/branch differentiation and those in which the meristem changes direction to produce both trunk and branch.^ref These depended on factors like whether the SAM is reproductive or vegetative, whether it grows vertically or horizontally, whether growth of the SAM is continuous or rhythmic (ie. has a period of dormancy or a growth pause) and the chronology of growth of each meristem.^ref

Below is an updated version which includes some models added later (and one which was removed as nobody found a real tree which conformed to the theoretical model).

https://gali-izard.arch.ethz.ch/francis-halle

Each architectural model has a unique combination of growth, branching, axis differentiation and position of sexual structures.^ref Not all of these are relevant to bonsai – as you can see Holttum & Corner don’t branch and Tomlinson & Bell branch underground. Many of these models are relevant for palms, cycads and tropical trees which aren’t commonly used for bonsai.

Two of the architectural models represent many of the trees used in bonsai at least in the Northern Hemisphere^ref – Massart’s and Rauh’s model – their main difference is in the branching angle with Massart’s at an angle to the stem and Rauh’s growing upwards. In both models the trunk is monopodial – it keeps extending upwards and is dominant.

Massart’s model represents Abies, Picea, Sequoia, Metasequoia, Cedrus, Taxodium, Taxus, Cephalotaxus, Ginkgo & Ilex aquifolium. More forms and discussion of Massart’s model are represented in this post.

Rauh’s model covers the Cupressaceae family (cypress, juniper & redwood), some Araucariaceae, the Pinaceae family including most Pinus species, the Podocarpaceae family, as well as angiosperms such as oak, maple and ash. This is shown in more detail in this post.

If you’re looking to understand the architectural model for your particular tree, you might consult this book – it mainly focuses on tropical trees but gives some pointers on working it out.

Some other models include Attim’s model for Eucalyptus, this is similar to Rauh’s model but follows a continuous growth pattern – in these trees as one leaf expands outside the bud it is replaced by a new bud initiated at the shoot apex.

Troll’s model is applicable for hemlock, acacia, beech, where “axes are all plagiotropic (ie. horizontal), the architecture being build by their continual superposition; main-line axes contribute part trunk, part branch, the proximal part becoming erected, most often secondarily after leaf fall” – it is believed that reaction wood is involved in determining this architecture (the type of wood created to stabilise a branch against gravity – compression wood developed under the branch in the case of gymnosperms, and tension wood developed above the branch in the case of angiosperms). Hemlock is a gymnosperm with this model.

Finally, trees can move from one model to another when they move from their juvenile vegetative phase to their reproductive phase. For example Apple has been found to conform to Rauh’s model when juvenile but Scarrone’s when reproductive:^ref

Angiosperm buds

Angiosperms (flowering trees) are more predictable in terms of their buds, because in addition to the terminal bud/s, in most cases a bud is also developed below a leaf petiole (stalk), and when that leaf falls off, the new bud grows from that position, known as the leaf axil (hence it’s known as an axillary bud). Therefore the bud pattern is equivalent to the leaf pattern or phyllotaxy.

It’s important to understand whether your tree has compound leaves, which have multiple leaflets.^ref These leaves only have one true petiole and at the base of this is where the lateral/axillary bud will form. No buds will form in the leaflet stems. See the below diagram.

https://www.bio1152.nicerweb.com/Locked/media/ch35/leaf_morphology.html

Variables in the phyllotaxy include the number of leaves per node and whether they spiral around the stem or not. According to an article in Nature^ref, at the shoot tip itself, the ‘golden angle’ is observed between leaves: 137.5° – in the article the researcher finds that this angle minimises the energetic investment of creating divergent leaf positions (in the creation of vascular tissue to supply the leaves). After the stem elongates, leaves start to spiral according to the Fibonnaci rule, whereby common leaf spiral angles are 1/2, 1/3, 2/5, 3/8 and 5/13. For example a 3/8 would mean the angle between leaves is 3/8 of 360^o, or 135^o. This means it takes 8 spirals before a leaf is in the same position on the stem (although now vertically separated).

https://greenlab.cirad.fr/GLUVED/html/P1_Prelim/Bota/Bota_typo_016.html

As can be seen above with only one leaf per node the arrangement simply spirals at different angles. With more than one leaf per node a similar principle applies but each pattern spirals (eg. both leaves in a two leaf per node spiral at the same angle). Multiple leaves at the same node is also called a whorl (common in gymnosperms).

So you should be able to predict where buds will develop on your angiosperm trees by simply looking at the leaf arrangement, and if it’s winter and your tree is deciduous, by the branch arrangement. What these buds will turn out to be – short shoots with flowers, vegetative shoots or flowers, is not as easy to understand but some pointers are here: Bud types – reproductive & vegetative.

Bud types – reproductive and vegetative

The reproductive system and organs of plants are extremely varied and complex, and worthy of an entire website to themselves – a comprehensive view is beyond the scope of this website. But what I want to do is provide a bit of information to help you identify which buds might be reproductive vs vegetative.

There are different buds for vegetative (shoots & leaves) and reproductive (flowers, strobili) organs – within each bud a different set of components develop depending on what kind of bud it is. For angiosperms, it’s hypothesised that flower buds are based on the same structures as vegetative buds – that is, a bud starts as vegetative and then differentiates into a flower bud.^ref For gymnosperms, reproductive buds contain male or female strobili.^ref These are the male pollen cones or the female seed cones.

There are two ways to work out which bud is which – by their appearance or by their position on the tree. The appearance route is best aided by dissecting some actual buds from the tree you are interested in, so you have real data from the real tree. Otherwise, read on for more information about how vegetative and flower buds differ in appearance.

Vegetative buds are “encased by strong, coarse, mature scale leaves. Thinner, more membranous scale leaves make up the next layer. The scale leaves form a protective enclosure surrounding the developing foliage leaves.”^ref In many of the articles online, leaf buds are said to be thinner than flower buds (at least for angiosperms). Below are the vegetative buds of Acer pseudoplatanus and Fraxinus excelsior^ref:

https://link.springer.com/book/10.1007/978-3-319-73524-5

A flower bud develops sepals, petals, stamen, pistil, ovaries & anthers, instead of leaves and more buds. Below is a scanning electron micrograph of a Bing cherry flower bud forming where M is the meristem, B is the bract and F is the very start of the flower forming – the progression over time is from left to right. On the right is the pistil with ovary (O) style (SY) and stigma (SM). The scale of the image is provided by the white bar on the bottom right hand side, which is 100 micrometres (or microns) – about 1/100th of a centimetre. Obviously it’s impossible to detect a flower bud at this stage by eye, it’s way too small!

http://treefruit.wsu.edu/when-and-how-to-reduce-doubling-in-sweet-cherry/

The buds of these Bing cherries started forming and were detectable under a microscope from mid-May (the location was Washington state USA) – the year before they would flower and fruit. At a lower magnification below is a progression in flower bud development of a Camellia – the key difference is that at A2 when the flower starts to differentiate, the tip of the bud becomes more rounded and flattens.

https://journals.ashs.org/jashs/view/journals/jashs/147/2/article-p104.xml

Some of the trees we use in bonsai are dioecious which means they are only male or female and not both^ref. This means they will produce only one type of flower or strobili bud. To check whether your gymnosperm is dioecious or monoecious you can check the gymnosperm database. Unfortunately I don’t have a reference link for angiosperms.

In gymnosperms there are no flowers, instead the reproductive organs are male or female strobili (pollen or seed cones respectively). A brilliant reference for some of these is available online here. An extract from the publication is provided below with some examples of vegetative and male & female strobili buds.

As noted another way to determine the type of bud is by its position. To do this you need to work out what the architecture of your tree is and where buds of different types typically form. Trees conform to one of 24 architectures as described in Tree Architectural Models and these give an indication to the location of reproductive buds. Trees can have one model for their juvenile phase (before they flower or adopt mature foliage) and then one for their reproductive phase.

In the case of apple, it has been found to conform to Rauh’s model when juvenile and Scarrone’s when reproductive^.ref Even with this, “great differences exist between cultivars whether they belong to “spur” vs. “spreading” or “terminal bearing” growth habit”^ref

In cherry, “The long branches bear short shoots, also called spurs, in lateral positions on the distal half or two thirds of the branch with more vigorous spurs toward the distal part [the most distant part]. Flowering occurs in axillary positions on the five to six basal-most nodes of all shoots whether long or short. Floral buds are thus located exclusively on the preformed nodes of the previous year shoots.”^ref

Red dots are flower buds, formed the previous year, and green dots are vegetative buds, formed during the growing season
https://www.frontiersin.org/files/Articles/105157/fpls-05-00666-r2/image_m/fpls-05-00666-g001.jpg

In some species, particularly pines, the long shoot buds have many different components on them in a specific order. Here is a Pinus contorta bud – you can see the male (pollen) cones appear first, and are positioned at the bottom of the final shoot, and the female (seed) cones appear last just below the top of the shoot.

https://www.researchgate.net/publication/271920043_The_pine_reproductive_process_in_temperate_and_tropical_regions

A similar layout is seen in Pinus thunbergii:

https://botanyboy.org/pinus-thunbergii-the-japanese-black-pine-tree/

As you can tell from the above, there is quite a bit of complexity in understanding the architectural model of a tree, and where different buds form, as there are many variables involved. Observation is probably going to be the better method.

Related posts:

Bonsai Tree Growth Stages

Most bonsai trees progress through stages of development, each with a different objective. In general the progression is thicken trunk -> achieve branch & root structure -> achieve branch, foliage & root ramification -> reduce leaf size -> evolve as branches grow/fall off. The faster we can move through the first few development stages, the faster we will have beautiful, well-proportioned bonsai – harnessing the tree’s natural growth is a way to speed this up. We also want to avoid doing things which slow down a tree’s growth during these phases, as this will mean it takes longer to get the tree we want. Read about how trees grow before starting at #1 below. Also consider what do old trees look like?

1. Trunk

Some bonsai enthusiasts collect mature trees for bonsai specifically so they can start with a thick trunk, following a collection process which minimises damage to the tree. The alternative is growing your tree’s trunk. Once a tree has its roots and foliage reduced in size in a bonsai pot, it won’t generate the energy needed to make significant sapwood additions and its girth will only increase by small increments every year. So you really need to be happy with the trunk size first before you stick it in a tiny pot. But – how big should a bonsai tree’s trunk be?

2A. Branch Structure & Overall Shape

Arranging the branches is what gives you the canopy and overall foliage shape that you’re after and the first step in this process is growing (or developing) the branches you want in the positions they are needed. Growing a branch starts with a new bud, which, unless it’s a flower bud, becomes an extending shoot and eventually a new branch. So firstly you need to work out where new buds will grow on your tree and then deal with the extending shoots as needed to get the required internode length.

You may need to remove some buds and shoots if they don’t help achieve the shape you are looking for – this should be done as soon as possible to avoid wasting the tree’s finite energy reserves. You have a trade-off to make here because leaving more foliage on the tree will provide more energy overall which contributes to its health and ability to recover from interference. However, growing areas of the tree which won’t be part of the future design is a waste of energy. You don’t want to remove so much of the tree’s foliage that it struggles to stay alive or develop the areas that you do want to grow out.

When you are creating your branch structure, often you will need to reposition branches – this is done with a wide range of different tools and techniques. A more advanced technique for adding new branch structure is grafting.

Sometimes the trunk itself or larger branches need a rework, to make them more interesting or to make them look more like old trees – for example adding deadwood or hollowing out the trunk. Usually this is achieved through carving.

2B. Creating a Strong Root System

The trunk thickening and branch structure phases both work best when the tree has lots of energy and so letting it grow in the ground or in a decent sized pot during these phases will get you there quickest. This also allows the roots to keep growing, but you want to understand about the role of roots, and root structure & architecture even if you still have your bonsai in a training pot. Particularly in this case, knowing about how to foster the the rhizosphere will help your tree stay vigorous. To maximise the roots’ exposure to nutrients and water you want to encourage Ramification of Roots (lateral root development).

Eventually it’s time to move the tree into a bonsai pot. This requires cutting back the roots, but as long as the roots are balanced with the foliage in terms of biomass, the tree should be OK. Root growth is usually prioritised outside of times of stem/foliage growth, and above 6-9 degrees C. So repotting might be best conducted at times that meet this criteria. Your growing substrate/medium is an important consideration.

3. Ramifying Branches & Foliage

Ramification is when branches subdivide and branch, giving the impression of age and a full canopy – and a well-ramified tree is a bonsai enthusiast’s goal. There are some techniques for increasing the ramification of branches and foliage. But not as many as there are for root ramification.

This stage also involves ongoing branch selection and reshaping (see 2A above). Another consideration is whether to keep or remove flower buds.

4. Reducing Leaf Size

An end stage in the journey to bonsai perfection is leaf size reduction. In nature, leaf sizes reduce relative to the biomass of the tree as it ages but since bonsai are small this effect doesn’t translate since the biomass never gets large enough. The tried and tested method for reducing deciduous tree leaf size is actually to practice one of the various methods of defoliation. A couple of others are covered here in reducing leaf size.

When to conduct these various activities depends on when the tree can best recover from them – which is a function of the Tree Phenology (or Seasonal Cycles).

5. Evolving Branches

Trees are not static organisms – they obviously continue to grow which is what we harness in the above steps. Part of this is that eventually branches may become too large for the design, or they may fall off (Peter Warren notes that Mulberry are known for this). As bonsai artists we want to have this in mind so that branches are being developed which can take their place in the future. This is an ongoing version of step 2A.

Growth Types Table

Fixed Growth (determinate) (leaves formed inside the bud before opening)	Free Growth (indeterminate) (leaves and buds continue forming throughout season)	Rhythmic Growth (a bit of both)
Ash Beech Hornbeam Oak Hickory Walnut Horse chestnut Pine Spruce Ginkgo short shoots	Elm Lime/linden Cherry Birch Poplar Willow Sweet gum/ liquidambar Alder Apple Larch Juniper Western Red Cedar Coastal Redwood Ginkgo long shoots Maple	Loblolly pine Shortleaf pine Monterey pine Caribbean pine Cocoa Rubber tree Avocado Mango Tea Lychee Citrus Olive Pinus radiata

From Thomas (2018) and RNET^R

Plant Growth Regulators (or Phytohormones)

You’ve probably heard of rooting hormone powder, or auxin, or gibberellins – these are all ‘Plant Growth Regulators’. Plant Growth Regulators used to be known as ‘phytohormones’ which means plant hormones. This has been quite a contentious topic among plant biologists.

A hormone in an animal is a chemical messenger, a substance which acts as a signalling or control molecule to cause an action to take place. “Hormones carry out their functions by evoking responses from specific organs or tissues that are adapted to react to minute quantities of them”^ref. In animals, hormones are produced at a specific site (a gland, like the pancreas), work at low concentrations, and have a predictable dose-response. That is, an increase in hormone will result in the more of the related action (eg. more insulin leads to more sugar being taken up by the liver).

There *are* substances synthesised by plants which are involved in regulating growth – plant growth regulators – but they don’t work in the same way as animal hormones. It’s said that the assumption that they did sidetracked plant researchers for decades.^ref Plant ‘hormones’ are synthesised in multiple sites in a plant (and potentially in every cell^ref), have multiple actions on different cells (they don’t act on just one organ or tissue), don’t exhibit predictable dose-response behaviour like animal hormones and are involved in significant interactions or feedback loops with each other.^ref

What this means is that it’s quite hard to unpick what they do and how they work. The roles and mechanisms of plant growth regulators are still very much current research topics, as can be seen at two of the research groups at Cambridge University’s Sainsbury lab^ref1,^ref2 Some of the early theories about them were comprehensively demolished in a seminal article by Anthony Trewavas^ref (in particular the theory of auxin-derived apical dominance which was later proven wrong as explained below).

We now know that plant growth regulators act in concert with genes and the proteins they express, and not as an independently acting substance (one of the genes involved in cytokinin synthesis is known as LONELY GUY…).

So what are the plant growth regulators, where and how are they made? There are nine main plant growth regulators you may come across in your reading:

Auxin^ref – classically called ‘the growth hormone’ and a signal for division, expansion, and differentiation throughout the plant life cycle – involved in root formation, branching, the tropic responses, fruit development, shoot meristem function, the development of cotyledons and senescence. The most common form is Indole-3-acetic acid (IAA). Auxin acts in a ‘ying-yang’ relationship with cytokinin (see below)^ref as well as with gibberellins. More about auxin below.
Cytokinins (CK)^ref1 ^ref2 – involved in cell division, shoot initiation and growth (including maintaining the stem cell niche), nutritional signaling, root proliferation, phyllotaxis, vascular bundles, leaf senescence, branching and nodulation, seed germination, nutrient uptake, and biotic and abiotic stress responses. 6-BAP or 6-Benzylaminopurine is a synthetic cytokinin which is used in micropropagation and agriculture. Coconut water (not milk) has been found to be a natural source of cytokinins.^ref
Brassinosteroids^ref – involved in a wide spectrum of physiological effects, including promotion of cell elongation and division, enhancement of tracheary element differentiation, retardation of abscission, enhancement of gravitropic-induced bending, promotion of ethylene biosynthesis, and enhancement of stress resistance.
Gibberellins (GA)^ref – involved in multiple processes including seed germination, stem elongation, leaf expansion and flower and fruit development.
Strigolactones (SL)^ref – induce hyphal branching of arbuscular mycorrhizal fungi and are shoot branching inhibitors.
Abscisic Acid (ABA)^ref – involved in the induction and maintenance of seed dormancy, stomatal closure, and response to biotic and abiotic stresses.
Jasmonates (JA)^ref – shown to be inhibitors of growth but also involved in development of flowers and defense responses against herbivores and fungal pathogens
Salicylic Acid (SA)^ref – associated with disease resistance
Ethylene^ref – multiple effects on plant development including leaf and flower senescence, fruit ripening, leaf abscission, and root hair growth.

Slightly maddeningly none of these substances do just one thing – they’re all involved throughout the plant!

So how and where they are made in a plant? This isn’t simple either. In fact local biosynthesis is thought to be critical for plants, whereby plant growth regulators are made at the site where they are needed. For example both auxin and cytokinin are synthesised in leaves *and* in roots^ref, and can be made by chloroplasts and mitochondria, organelles which occur throughout the plant.^ref Chloroplasts can make precursors to auxin, abscisic acid, jasmonates and salicylic acid.^ref

Even though plant growth regulators don’t act in a predictable dose-response way like animal hormones, they still have a role in shaping plant growth in tissues which are sensitised to respond to them. Theoretically by understanding these responses we can manipulate a tree’s growth. And this is what they do in plant tissue culture (more on that below).

You may have heard the theory of auxin-controlled ‘apical dominance’, which holds that auxin produced by leaves at the apex inhibits lateral buds. This theory was strongly criticised by Trewavas in 1981: “The only hypothesis of apical dominance which has retained some measure of support is the nutritional one. A number of plants placed under conditions of reduced nutritional status adopt a growth pattern of strict apical dominance.” His point of view was further supported by a 2014 study which found that “sugar demand, not auxin, is the initial regulator of apical dominance”.^ref The researchers found that after removal of the shoot tip, sugars were rapidly redistributed over large distances and accumulated in axillary buds within a timeframe that correlated with those buds releasing. But auxin didn’t travel fast enough to be responsible for bud release. So basically they found that apical dominance arises because the main shoot is greedy for sugars, and due to its position at the end of the vascular system it can prevent lateral buds from taking the sugars needed to release and grow.

Auxin does play some role though, and the theory is that its role related to the fact that it’s the only plant growth regulator which displays polar transport. That is – it moves from the apex to the base of the plant, via the phloem, and can travel the entire length of the plant, ending up in the roots. This gives auxin a special role related to the spatial aspects of growth, and auxin ‘maxima’ (locations where auxin accumulates) are sites where new buds, flowers or lateral roots emerge. In fact, auxin and cytokinin work in concert throughout the plant, from shoots to roots, with apparently opposite effects in each location “like yin and yang”.^ref

An excellent reference point for this subject is the world of plant tissue culturing. This is where small pieces of plant tissue are sterilised and cultured in a medium containing plant growth regulators, which cause the tissue to grow into a ‘plantlet’ (sometimes in a test tube, if the source material is small). Further steps multiply the plantlet into several plantlets, which are then encouraged to create roots, multiplied again and/or planted out as seedlings to harden off. This process is used for industrial plant cloning where large numbers are required, and in the aquarium trade to avoid contamination with snails and other microbes (see Tropica’s website).

In plant tissue culturing, plant growth regulators are used to induce the relevant growth stage, which ones work for each species in which stage is documented in the ‘protocol’ for that species. In all cases specific ratios of cytokinin:auxin (and sometimes gibberellins) lead to different developmental stages – shoot growth, lateral shoot growth and root growth.^ref1,^ref2 To give you a bonsai-oriented example, one study determined a protocol for the micropropagation of Prunus Mume^ref. They were able to multiply fresh prunus mume shoots in a petri dish using a 4:1 ratio of cytokinins to auxins, and then root them using auxin.

So – apologies for the rather long read, it is quite a complicated subject! What can we take from all this for our bonsai practice? Firstly we can stop the brain-bending trying to understand how auxin controls apical dominance because it doesn’t – access to sugars does this instead.

Also we can use the yin-yang rule – high cytokinin:auxin encourages buds & shoots, and high auxin:cytokinin encourages roots. So I’m going to start adding some auxin rooting gel into my air layers and cuttings. Cuttings have never worked for me in the past so maybe this will be the secret sauce I need. I’m also going to try some cytokinin gel to encourage lateral budding on my trees.

If you are looking for products to give this a try, make sure the product actually contains the plant growth regulator you want. For example, Clonex contain auxin, and some of the orchid budding pastes such as Keiki paste contain Kinetin (a cytokinin). Many other ‘rooting hormones’ or plant hormones products on the market have no ingredient list at all, so avoid those. You can also find these products online in shops dedicated to hydroponics, where cloning and plant tissue culturing is a technique used by practitioners, or in lab supply shops such as microscience or Phillip Harris in the UK. You can even make your own hormone gels following these instructions.

Another trick you can use is that gibberellic acid can be used to break dormancy in seeds, if you really don’t have the patience to wait for natural dormancy to break. Or give coconut water a try, this has been found to have a similar effect in a range of species. For hard coated seeds in particular, usually it’s best to search Google Scholar for a researcher who has experimented with different approaches, since what works is very species-dependent.

Epicormic Buds

There are a few different terms bandied about to describe buds which pop up in unexpected positions on a tree – ‘adventitious’, ‘dormant’, ‘suppressed’ ‘preventitious’ ‘proventitious’. Epicormic growth is actually just growth which forms on old-growth units of the tree – not in the current season’s growth.^ref It’s great for bonsai because it helps keep the foliage condensed and well-ramified and allows you to develop branches which are closer to the trunk, to keep the profile compact.

This study proposes standardising on the terms ‘adventitious’ and ‘preventitious’. The key difference between the two types is how they develop – preventitious buds originate exogenously (due to an external trigger) and descend from a shoot apical meristem, while adventitious buds develop endogenously (due to internal triggers) from previously non-meristematic tissue.^ref

A key concept here is that of the meristem which we encountered back in How trees grow. A meristem is an area in a plant containing stem cells – cells which can become any other type of cell. Trees maintain four active meristems which are continuously producing new stem cells as well as differentiated cells used to build the plant (the shoot apical meristem, the vascular cambium, the cork cambium and the root apical meristem). These allow the plant to respond to damage by growing new organs. The different types of epicormic buds arise from epicormic meristems, which are traces of meristematic tissue which are not located in the active portions of the above-ground meristems.

Preventitious buds arise from meristematic traces which are triggered to become full buds and sprout at some point in the future, for example if the tree is wounded or damaged and needs to generate more foliage for photosynthesis. In fact these preventitious meristems may come from axillary buds which aren’t activated during their growth season. Particularly in angiosperms, many more buds are generated than are activated in a growth season, and these buds may stay dormant until needed. Not only that, but mature buds approaching bud burst have tiny buds inside them as well, which become next season’s buds if a bud extends. If it doesn’t extend, there are 2 years of dormant bud tissue available for future activation.^ref

Adventitious buds happen when a callus or other wound response creates meristematic tissue which connects to vascular growth (eg. the cambium) and establishes a trace similar to preventitious buds. In the future this trace can become a shoot.

This study identified four different strategies for epicormic bud development – external clustering, isolated buds, detached meristem and epicormic strands.

External clustering is where “trees produce relatively small, persistent axillary buds, which develop into epicormic complexes consisting of numerous buds and shoots”. Even though they are not visible, every year they extend with annual growth creating more meristematic tissue and/or leaf primordia (embyonic leaves), and sometimes shoots as well. These bulges on tree trunks are a familiar sight on many trees – such as this Linden tree near my house:

The majority of species which are known to be prolific producers of epicormic shoots fall into the external clustering strategy. I often see Oak trees in Richmond Park with rounded protuberances on their trunks – these are epicormic complexes under the bark.

The isolated bud strategy is the “initial production of larger external epicormic buds, mainly high buds, which are less persistent and less likely to form large clusters.” These buds are buried in the bark, or in the case of gymnosperms a meristematic ‘bud base’ is left in the bark.

The detached meristem strategy is also observed in conifers and involves “the maintenance of minimally developed meristems hidden in leaf axils” which require some trigger (like fire) to become active. These meristems are not connected to the vascular system but can connect later when they create buds. Members of the Araucariaceae family have been found to use this strategy, such as the Hoop and Wollemi pines.^{Ref1, Ref2}

The final strategy is epicormic strands “characterized by the presence of extensive meristematic strands within the bark that are capable of producing a continuous series of ephemeral epicormic buds” – this is observed in Eucalyptus.

One key point is to understand why a tree develops epicormic buds into shoots – and the answer to this is that is a response to stress – stressors can include insect defoliation, fire, frost, wind damage, disease, drought , intense competition, low site quality, bole orientation, vascular embolisms and heavy pruning.^ref The bad news is that epicormic branches have a reputation for being weaker and not very long-lived. In his book the Wild Trees Richard Preston references epicormic branches on Coast Redwoods, noting that the people who climb these trees avoid putting weight on epicormic branches since they are liable to shear off the tree.

To work out where epicormic buds might appear on a tree, go back and read Buds, as preventitious buds in particular will develop in places where buds could have formed in previous growth period.

Gymnosperm (Conifer) Budding

Gymnosperms relevant for bonsai include ginkgo and the Pinales order (Araucariaceae, Cephalotaxaceae, Cupressaceae, Pinaceae, Phyllocladaceae, Podocarpaceae, Sciadopityaceae & Taxaceae – this is explained in The kingdom Plantae and where trees fit in). Ginkgo is a special case described separately at the end of this post.

So what we’re interested in in bonsai is where lateral buds appear, and in particular whether they can develop adventitiously (or backbud). Angiosperms (flowering plants) are relatively easy to understand in terms of their lateral budding, as many species reliably produce a bud in each leaf axil (the axil is the place on the stem where the leaf is/was connected). In gymnosperms though, this is not as predictable and it’s not the case that each needle contains a bud – at least not in every species and not detectably. And looking at the different foliage forms below, you can see that different bud types must be involved to generate all these different leaf models.

https://cmg.extension.colostate.edu/Gardennotes/134.pdf

Many conifers have a terminal bud at the end of each long shoot/branch surrounded by a number of close lateral buds in what’s called a ‘whorl’. These include pines, spruce, fir, and the Auracaria family. The whorl in the picture is a Scot’s Pine, with a vegetative bud in the middle and reproductive buds around it. This will usually be the apical or strongest bud, receiving the majority of the sugars from photosynthesis.

https://joshfecteau.com/meet-the-pines-scotch-pine/#jp-carousel-8472

When the vegetative bud extends, it is called a ‘candle’ because it is a long thin structure – which looks like a candle. Below you can see a Pinus Thunbergii (Japanese Black Pine). Some candles are extending and some have extended and formed cones from the lateral buds around the main bud. No branching will occur from reproductive buds as they terminate the shoot.

https://www.conifers.org/pi/pi/t/thunbergii02.jpg

Bonsai enthusiasts commonly prune the candles to maintain a short needle length, this has the effect of arresting the needle growth; it is also possible to completely remove the candle, to force bud break at the base of the candle which results in smaller and more buds. In pines there are usually short shoot buds at the base of the candle – these will produce needle clusters in the future but no stem elongation. Breaking or pruning the top of the candle will activate these buds, which is good for ramification. If you want to continue developing the structure of the tree, you need a long shoot with a terminal vegetative bud as this won’t fall off.

As well as the terminal buds, pines sometimes have buds on their lateral shoots, between the needles, as well as internodal buds, which appear along the stem and not just at the end. These usually appear at the axil of the individual leaves on a long shoot/stem (Dörken, 2012).

Other conifers such as those in the Cupressaceae family (Thuja, Juniperus, Cypress) do not have whorls or needles, they have scale-type leaves in ‘branchlets’ (and needle-like leaves when juvenile). You can see below some examples of these which show the lateral buds forming from inside the lateral leaves (the leaves on the sides of the shoots). Since these branchlets squeeze a lot more leaves in, they have more potential for budding than do individually-leaved species such as Abies (fir) and Picea (spruce).

https://craven.ces.ncsu.edu/2022/03/conifers-with-scale-like-leaves-what-makes-a-leaf/

However one key attribute of species in Cupressaceae like these scale-leaved ones above is that just like pines they do still have differentiated short shoots and long shoots (Dörken, 2012). The short shoots are the individual branchlets, which abscise as a unit after a few years (detach from the long shoot and fall off). At the base of this short shoot is another bud waiting to generate a new shoot once the branchlet falls off. So new foliage will come from the leaves on the branchlet while it is active, and then from where the branchlet was connected to the stem when the whole branchlet falls off.

Conifers with individual needles such as firs and spruce, and needle-leaved junipers, have buds at the base of each leaf, but tend to bud towards the end of the most recent growth. Last year we dug up a Christmas tree from our allotment and I pruned the ends of most of the branches because it was too wide to fit into the house. The effect of this has been to stimulate the subordinate branches to bud – but again this has only happened at the ends of the branches (see below). Something about firs & spruces keeps the active budding zone at the end of branches.

As well as understanding the budding pattern, a key question for bonsai afficionados is whether or not a particular tree will backbud. That is, will it be possible to increase ramification and foliage density by encouraging axillary or adventitious buds to form.

Gymnosperms were traditionally believed not to resprout, with research in the past finding that buds are not present in leaf axils of conifers. Despite that, there are quite a few gymnosperms species which do, including the following. Some of these “do not have distinct buds at all; they produce new growth from meristematic tissue hidden under the skin of the twig” (Thomas, 2018) – this is known as an epicormic bud. This may be a false distinction since the meristematic tissue may just be early buds which are not developed enough to be visible.

Some Abies (fir)^ref including Abies nordmanniana^ref
Araucaria & Agatha species including including Hoop Pine^ref and Wollemi pine ^ref1, ^ref2
Cedrus (true cedar)^ref
Cryptomeria japonica (Japanese cedar)
Ginkgo
Juniperus^ref
Larix (larch)^ref
Metasequoia glyptostroboides (dawn redwood)
Pseudotsuga (Douglas fir)
Some Pinus (pines)^ref – but pines are notorious for losing their ability to bud anywhere other than on the most recent 1-2 years old stems. Brent Walston at Evergreen Gardenworks says with Pinus thunbergii that as long as there is still a living needle on a stem, if you cut the stem above it, that will force a bud at the needle axil.^ref This lines up with the idea that buds in pines are present under the leaf axil of long shoot leaves.
Taxus baccata (yew)
Sequoia sempervirens (coast redwood)
Sequoiadendron giganteum (giant redwood)
Taxodium distichum (swamp cypress – deciduous)^ref
Thuja occidentalis (sometimes called White cedar)
Thujopsis dolabrata (a Japanese species similar to Thuja)

So actually there are quite a few!

Some studies have indicated that “cytokinin sprays on conifers growing in the field can
increase the number of visible axillary buds^“ref and as a result this study concludes that “conifer leaf axils might not be as blank or empty, at least in recently initiated shoots, as they might appear to be. Cells in the leaf axils, while not forming buds, can maintain a meristematic potential and if they lose meristematic appearance, they may be
preferentially able to dedifferentiate into bud forming structures.”^ref

In ginkos^ref, axillary buds are present in the nodes of long shoots only, and these trees can backbud – below is an example of a ginkgo at the Seattle Japanese Garden – you can see new leaves sprouting from the bark of a well-established tree (from the longest long-shoot of all – the trunk).

I’ve also spotted this tree around the corner from my house in London – it was quite tall with all the foliage at the top of the tree – when I saw it cut back so severely I was sure it would die. There were only the tiniest of shoots here are there on the trunk. But in a matter of a few weeks it grew back profusely, which makes me think it must be a Thuja of some kind – perhaps Thuja occidentalis ‘Golden Smaragd’.

Finally another lovely example of conifer resprouting are the amazing dai sugi in Japan – these are Cryptomeria japonica which are cultivated for forestry purposes. The tree is encouraged into a multi-stem form with horizontal branches, which sprout new vertical stems. These are harvested over and over, and new stems grow. In this way the same tree has been used for forestry for hundreds of years without killing the tree. The technique is explained in Jake Hobson’s book Niwaki, which also includes a brilliant photo of bonsai dai sugi, which I think look bizarre but amazing. I have several Cryptomeria japonica at my allotment in the hope of creating something similar (although realistically the ones in this image are probably air-layered).

https://twitter.com/wabisabi_teien/status/1038034988841627648?lang=zh-Hant

Tree Phenology (or Seasonal Cycles)

The term phenology is used to describe the life cycle of a biological organism like a tree. Phenological events for trees include bud development, bud break, flowering, fruiting and leaf & fruit drop, as well as other unseen changes such as sap rising, seed development, root growth, cambial activity or hardening off of tissues for winter.^ref

Tree phenology is entwined with the environment in which the tree lives. As there are a very large number of different climates and micro-climates within them, there are accordingly many different nuances in tree phenology, according to the location and environment. Even the same species can show widely different phenology between two different places (at least from a timing point of view).

So to really understand how phenology would play out for your own trees, you need to understand the species phenology and how it varies based on location. You’ll often find bonsai articles are specific to the location of the author which won’t always be relevant to you.

The main phenological events relate to a tree’s growth and reproduction. For example, roots stop growing below 6°C, buds break when the tree detects a low chance of frost in the future (which might damage the tender buds and shoots), photosynthesis, energy production and growth is highest when there is the most sun, and reproduction happens in conditions which most favour seed survival.

In the boreal forests – “high-latitude environments where freezing temperatures occur for 6 to 8 month”^ref phenology is mainly driven by temperature, affecting the timing of the start of the growing season and thereby its duration^ref
Temperate-zone forests are located between the tropics and the boreal forest zone – they have hot summers and cold winters with high temperature variation^ref, and their phenology is also mainly driven by temperature^ref
Mediterranean coniferous forests are mainly driven by water availability^ref
Australian ecosystems are extremely diverse and also subject to irregular events such as fire, drought, cyclones and flooding, which can affect phenological events, but a key driver is water availability.^ref Where evergreens dominate in this ecosystem, flowering is the main phenological event.
In tropical forests which have less variation in temperature and usually high water availability, leaf shedding and growth is continuous, but reproduction (flowering and fruiting) demonstrates ‘mast’ timing effects associated with drier than normal conditions^ref (ie. all trees fruiting at the same time every seven years)

In boreal and temperate areas the phenology is described in this article and summarised in the images below. But if you’re keen to understand the specific phenology for your tree in your area, you could consult google scholar.

The chart below shows the proportion of Eucalyptus loxophleba flowering at any given time in a seed orchard in the southwest of Western Australia. The highest proportion of flowering happened in spring (Sept-Nov in Australia) but a significant portion also happened in winter (June-Aug). Flowering fell to zero in the hot, dry summer (Dec-Feb).

https://www.nature.com/articles/s41598-020-72346-3/figures/2

This all seems a bit confusing given how many different variables there are, but there are some basic principles you can use from a bonsai perspective:

Trees in their growth phase (usually when there is plenty of sun and water) will be able to recover more easily from significant damage (such as large trunk chops or carving wounds) and fight any pathogens which might seek to take advantage of these.
Similarly leaf pruning during active growth will result in more buds activating.
Trees which are in a strong vegetative growth phase (growing leaves and stems) deprioritise root growth. Root growth gets a turn after the leaves establish.
Trees which have set buds but haven’t flowered yet – if you prune indiscriminately – you will lose flowers! There is a way to identify flower buds on your tree but it involves a bit of effort. Flower buds differentiate from vegetative buds at a certain point prior to flowering/leafing out. You can identify different looking buds on your tree, then remove one example of each. Cut it open and look at it under a loupe or microscope and you will be able to see which one was the flower vs the leaf or shoot. Or if you’re both patient and organised, take a picture of some your tree with buds and then with flowers – and you should be able to see what the different bud shapes are.
Storage of carbohydrates to storage tissues will take place during growth phases, and these will be used in turn when less photosynthesis is happening, to drive respiration and other processes requiring energy. Read more about how storage varies in roots here: Root Food Storage (or, can I root prune before bud break?)
If you’re a fan of wiring, doing this before a stem hardens off will allow you more bendability (although watch out for growth around the wire)
Depriving a tree of resources (water, nutrients) will mimic ‘hard times’ and cause it to respond accordingly phenologically – drop its leaves earlier, produce less flowers/fruit or not flower at all, or push out emergency growth (like adventitious buds/suckers)
I think it’s important to say that although the term ‘dormant’ gets used in relation to trees, this is a little misleading. Trees are living organisms and still need to maintain their metabolism even during winter. This includes respiring (using oxygen and stored energy to maintain metabolism), photosynthesising (for any tree with green areas remaining including evergreen trees but also deciduous trees with green stems), transpiring (even deciduous trees still transpire during winter, although a lot less than when they have leaves and in particular they take up water to swell the buds prior to bud break^ref), and taking up nutrients through the roots. As I’ve written elsewhere in this site, root growth can happen above 6 degrees C, so your tree may well be more ‘alive’ than you think during winter.

I know there will be people saying at this point – just tell me what happens when!! For those people here are some general guidelines for temperate zones.

You can expect conifers to cease xylem production in autumn and root growth in winter, and to pick these up again between 2-7 degrees C (cambium) and 6-9 degrees C (roots). Buds will burst from early spring onwards depending on the species and latitude and pollen cones will release their pollen. Seed cones will start maturing, which can take just one summer (Picea, Tsuga) or one or more years plus the summer (Pinus, Cedrus). Next year’s buds and future years’ seed cones will form in late summer, and old needles (2+ years depending on species) will drop in late autumn. Mature seed cones will drop or release seed from late autumn onwards. ^{ref1 ref2 ref3} Hardening leaves for the winter also happens in late autumn.

The main differences for angiosperms in temperate zones revolve around xylem production, leaf growth and senescence within the season, and flowers & fruit. In spring xylem creation will commence – in diffuse porous trees buds can break earlier but ring porous trees need to create the new season’s xylem layer before budding. Some trees will burst bud based on temperature and others on photoperiod (or a combination of the two).^{^ref} Whether flowers or leaves come first depends on the species, and the timing of flowers is hugely variable (Frank P Matthews has a list of flowering times for ornamental trees in the UK). The leaves of deciduous trees start a structured senescence process in the autumn, when they remove cholophyll and other molecules from the leaves for storage and recycling (hence the colour changes). After this has been completed the tree creates a cork layer at the base of the leaf causing it to drop off. Fruit develops throughout the growing season and depending on the species will drop off from early summer through to winter.

There’s one more phenological domain which I haven’t covered in this article – the phenology of the microbiome. This is a whole other kettle of…microbes…and might be the subject for a future post.

Finally, the fabulous In ‘Defense of Plants’ podcast has covered phenology in this podcast episode.

Should I remove flower buds or fruit?

That depends what tree you have and what you are trying to achieve. Obviously if you have satsuki azalea, you probably want to leave the flowers on the tree! If you have a crabapple, personally I don’t think there is much point if you don’t let a few fruit form. And I am really partial to rose-coloured larch cones. All trees form some kind of reproductive organs, whether they be conifers with their strobili (cones, either pollen or seed forming), ginkgo with their ovules, or angiosperms with their flowers and fruit. Some are almost unnoticeable and others are right in your face. Bonsai wisdom sometimes says these should be culled or removed entirely in order to avoid draining the tree of its energy.

When considering this question we need to understand the idea of resource ‘sources’ and ‘sinks’ in plants. A source is a material producer and exporter, and a sink is a material importer and consumer.^ref See the below table for sources and sinks in trees. As you’d imagine, leaves are a major source of carbon and a sink of inorganic nitrogen (nitrogen as a macronutrient). Roots are a source of inorganic nitrogen and leaves are a sink. So what about fruit, seeds, and flowers, which supposedly drain the tree? As you can see they are major sink organs – but not only sink organs…they are also source organs!

https://academic.oup.com/jxb/article/68/16/4417/3002648

Let’s have an interesting little diversion – did you know that it’s not only leaves which photosynthesise? This fascinating study^ref looked at the photosynthetic activity of (a) ears of wheat (b) sycamore seed pods (c) a green tomato (d) unripe and ripe strawberries (e) a greengage (f) unripe cherries; and (g) a green apple. The images below were taken using fluorescence imaging and anything with a colour indicates that there is photosynthesis taking place – with the red and orange areas the strongest. Check out the sycamore seed pods!

https://onlinelibrary.wiley.com/doi/full/10.1111/tpj.14633

How the heck can this happen – well there are various theories about the mechanism (including recycling CO₂ from respiration, and the presence of stomata on fruit) but the point is that maybe seeds and fruit, particularly if they have periods when they are green, don’t act as such as sink as we might think, and for a period are acting as a source and not a sink.

This study states that “reproduction in Beech does not deplete stored carbohydrates, but it does change the amount of nitrogen stored” and this study found that “fruiting is independent from old carbon reserves in masting trees”^ref which basically means that fruit uses current year photosynthates/energy and doesn’t actually deplete reserves.

On the other hand this study found that Douglas fir tree rings were narrower in years when they bore many seed-cones^ref and this one mentions that “experiments with apple trees have shown that roots can die from lack of carbohydrate supply when they are over cropped”^ref

All living things have processes for managing and balancing resource allocation^ref and this is likely an evolutionary differentiator. In trees, resource availability limits the amount of fruit which is allowed to develop – even pollinated flowers may not develop into fruit if the tree does not have enough resources available – these could include energy, or nutrients.^ref So to an extent the plant itself manages the resource allocation.

To complicate matters further many trees use a ‘masting’ strategy for reproduction, which means they have years where many more seeds are produced, often synchronised with other trees of the same species. One theory for how this happens is that the weather influences how pollen is distributed – in beech windy conditions lead to mast years whereas in oak short pollen seasons do.^ref Temperature and precipitation also affect pollen production and distribution (high temperature increases pollen production but high precipitation washes it away).^ref In this study on Japanese oak, “high seed production never occurred in two successive years, but successive years of low abundance were observed several times between 1980 and 2000.”^ref

Overall there are a lot of factors interacting when it comes to reproduction. Photosynthetic seeds or fruit can contribute to carbon production, and may use only current year photosynthates, so the tax may not be as high as thought, but there is some evidence that reproduction can divert energy from roots and foliage.

If you are really focused on trunk growth, branch structure or foliage development on your bonsai tree, you might want to divert the energy from reproduction to these areas by removing some or all reproductive organs, until you are happy with the trunk/foliage. At this point then you could then let the tree reproduce (noting that removing cones one year will cause more cones to develop the following year)^ref.