The multiple functions of tree bark

Laura Ducatez-Boyer1*, Pauline Majourau 2*

Abstract Bark provides many functions for trees. Bark plays an essential role in transporting photosynthetic products in plant tissues. Bark is also crucial to the mechanics of the stem. Furthermore, bark is involved in defense against herbivory, protects against fire, and provides insulation in cold conditions. Other functions related to storage of water, metabolic regulation, or wound healing contributes as well to the life of trees. These functions of the bark are linked to its complex structure. Bark structure is well known and is defined as the whole tissue beginning from the vascular cambium and running until the rhytidome. A high variability of bark tissues morphology exists between species, which may indicate its importance in tree processes and highlights its role in plant ecological strategies.

Keywords Bark, bark function, tree physiology, tree mechanics, tree protection.

1 Université de Guyane, UMR EcoFoG, BP 316, F-97310 Kourou, French Guiana. 2 Université des Antilles, UMR EcoFoG, BP 316, F-97310 Kourou, French Guiana. * Corresponding author: [email protected], [email protected]

Contents Tree barks is morphologically diverse, which could be the result of specific ecological strategies. This diversi- ty might also be the result of adaptation to environmental Introduction 1 conditions, fire resistance, or insect attacks. This morpho- 1 Bark: diversity, anatomy, nomenclature and logical diversity and its causes remains poorly understood composition 1 (Paine et al., 2010). 1.1 The diversity of barks 1 1.2 Woody stem anatomy 2 First, bark anatomy will be described. Following this 1.3 Bark structure and composition 2 we shall discuss the physiological, mechanical and protec- 2 The role of bark in tree physiology 3 tive functions of the bark. These roles of the bark are 2.1 Sap flow: sugar transport and tissue covered in three parts. (1) Physiological aspects of the communication 3 bark. Notably, bark contributes essentially to sap distribu- 2.2 Water storage 3 tion in the plant. (2) The mechanic function of the bark, as 2.3 Storage and exchanges of water and gases 3 a support for the tree for example, is dealt with in the 3 Stem mechanical support 4 second part. (3) Finally, the protective function of the bark 4 Protective function of bark 4 discussed in the third part allows us to comprehend how 4.1 Protective mechanisms and adaptations of bark 4 bark can avoid damage to the tree. The final section is dedicated to discussing the idea of tradeoffs between the 4.2 Bark self-repair mechanisms 4 multiple functions. Discussion and conclusion: trade-offs of functions in bark 5 Acknowledgements 5 References 5 1 Bark: diversity, anatomy, Appendix 7 nomenclature and composition

1.1 The diversity of barks

Introduction Commonly, bark is viewed as the dead, touchable A tree is an organism at least 7 meters high (as de- surface of trees that covers the trunk. In botanic terms, fined by the Food and Agriculture Organization of the bark is actually a complex living tissue made of several United nations (FAO)). All trees have stems and branches layers. Bark tissues display a diversity of appearances and composed of an internal wood tissue. This wood is cov- textures, thickness and shapes (Figure 1). ered by bark with a percentage of 9 to 15% of the stem volume (Harkin and Rowe, 1971). Other organisms have barks (such as vines), however in this paper we refer only to the bark of trees. The multiple functions of tree bark —2/7

Figure 1 – Cross-sections illustrating bark variation between different species: (a) Buchanania obovate, (b) Brachychiton paradoxus, (c) Lophostemon lactifluus, (d) Planchonia careya and (e) Alstonia actinophylla. Bar, 1cm. (Modified from Rosell, Gleason, Méndez-Alonzo, Chang, & Westoby, 2014).

This diversity of bark appearance is probably im- portant. If these differences in bark morphology were not important, all species should have the same bark, with the same characteristics. There is no clear explanation for this diversity (Paine et al., 2010; Rosell, Gleason, Rodrigo, Chang, & Westoby, 2013). Scientists have defined a suite of measurable bark traits and try to comprehend how changes in these traits explain the performance of an or- ganism. The effective correlation may justify the mainte- nance of a particular morphology in a particular species. Figure 2 - Bark anatomy. Bark is composed of different tissues. These tissues are the rhytidome, the periderm and the phloem. A: 1.2 Woody stem anatomy Radial arrangement of bark tissues in the stem. B: Details about layers structure (Modified from Leite & Pereira, 2017). In order to explain bark variation in different species The multiplicity of designations associated to the of trees, the anatomy of woody stems must be understood. different layers can be confusing. The different Stems of a tree, trunk included, are composed of wood names attributed to theses layers in the literature is sum- and bark. Both wood and bark are associations of several marized in a table at the end of this document (Appendix kinds of tissues. Two radial meristems, called cambium, – Table I). produce the different tissues inside the stems of a tree (Leite & Pereira, 2017). The most inner cambium, the vascular cambi- 1.3 Bark structure and composition um, synthesizes two different tissues, one in the inside flank and one in the outside flank of the cambium which are respectively: the xylem (heart wood) and the second- The potential functions of bark may also partially ary phloem. The outer cambium, the cork cambium, also been explained by the specific cellular arrangement of called the phellogen, produces the phelloderm towards bark and the chemical components included in its cells. the interior and the phellem (also called suber or cork) Details about three tissues are given. towards the exterior of the cork cambium. The phellem, or cork, is a foam, made of dead par- Altogether, phellem, phellogen and phelloderm con- enchymateous cells with empty lumens. This tissue is stitute the periderm (Leite & Pereira, 2017). The phloem mainly composed of very regularly closed arranged hex- is divided into functional parts (non-collapsed phloem), agonal prisms cells which represent 90 to 95% of the total and non-functional parts (collapsed phloem). The succes- volume of cork. These cells are the earlycork cells sive layers of dead periderms associated with non- (Pereira, 2015). The tightly-packed organization of these functional phloem layers constitute the rhytidome (also cells forms a compact structure without any intercellular called the outer bark) (Angyalossy et al., 2016; Leite & spaces. The apparent regularity of the cork's structure Pereira, 2017), this is the outermost layer of bark. made by the earlycork cells is broken off by the yearly growth of latecork cells. These few latecork cells, which Bark which represents approximately 10 percent of are smaller prisms with a thicker cell wall than the ear- the log volume (Harkin and Rowe, 1971) is constituted of lycork cells, lead to the formation of seasonal rings. multiple layers which are, successively from the inside to the outside of the stem: phloem, periderm and rhytidome Moreover, in function of the species, numerous and (Figure 2). The bark is also defined by the International sometimes large lenticular channels can also be visible in Association of Wood Anatomists (Angyalossy et al., the middle of cork tissue and interrupt its regularity (Leite 2016) as all tissues outside of the vascular cambium. & Pereira, 2017). The multiple functions of tree bark —3/7

The phellem is also characterized by the two main The presence of such molecules, like RNAs or pro- components of its cell wall: suberin and lignin. Cell walls teins in phloem sap could explain its role in physiological of the phellem contain 53% suberin. Suberin gives im- regulation and responses (Ruiz-medrano, Xoconostle- permeability, resistance and compressibility properties to cázares, & Lucas, 1999). For example, proteins such as the cells. And Lignin, the other important component of jasmonic acid are essential for leaf recovery and are found the phellem cell wall represents 26% of the whole cork. in the sieve tubes (Zhang & Baldwin, 1997). Lignin is an aromatic polymer with a remarkable three- Phloem may allow essential communication between dimension molecular structure which confers strength to plant tissues in defense processes, growth mechanisms the cell wall (Pereira, 2007, 2015). and probably other important pathways like environmental The phloem, another tissue of the bark, is composed adaptation (Divol, Thibivilliers, Kusiak, & Dinant, 2005). of different specialized cells: the companion cells, the sieve-tube elements and the parenchyma cells. All these cells are interconnected through plasmodesmata and each of them carries out a distinctive function. The parenchyma 2.2 Water storage cells produce nutritive resources. The companion cells are specialized parenchyma cells, necessary for the mainte- Water storage capacity is defined as the amount of nance of the enucleate sieve elements. And the sieve-tube water that can be withdrawn from a compartment to an- elements form the path for sap flow (Angyalossy et al., other in case of water potential changes (Scholz et al., 2016; Rennie & Turgeon, 2009). 2007). Bark wettability or bark water storage exists and Phelloderm tissues are mostly composed of paren- allows water to be released to the rest of the tree when chymatous cells, these cells are rarely specialized and water needs increase. This water storage capaci- usually not suberized. These cells differ from cortical cells ty (principally in outer parenchyma (Scholz et al., 2007) (phellem) by their radial alignment and may perform the appears to be crucial to prevent drought damage and re- storage of photosynthetic products (Angyalossy et al., duce loss of water from evapotranspiration (Levia & 2016). Herwitz, 2005). This water storage is an important factor in plant– water relations, this mechanism differs significantly among tree species and is linked to bark morphology and branching architecture, and to the geoecology of 2 The role of bark in tree trees (Scholz et al., 2007). For example, increased bark physiology thickness contributes significantly to greater water storage (Rosell et al., 2013). As we saw, bark has a complex structure. This struc- ture permits many functions for tree functioning and we first interest to physiological benefits for tree from the 2.3 Exchanges of water and gases bark. These functions are manifold and comprise the sap flow in the inner part of bark and the water storage in the outer part of bark. But bark also plays a role in the ex- Lateral water and gas exchanges can occur in changes of water and gases, and permit sometimes photo- bark. Phellem tissues are involved in these transports. synthesis. The phellem is made up of multiple layers of dead cells and waxes, and provides the barrier for water and gas transfer (Lendzian, 2006) but in certain species, the phel- 2.1 Sap flow: sugar transport and tis- lem is interspersed with lenticels, aerenchymatous cork sue communication areas which are paths for the exchange of water vapor, oxygen, and carbon dioxide between the tree and the at- mosphere (Lendzian, 2006). These lenticels are multicel- Phloem is the path of circulation for phloem sap. lular structures and functionally analogous to stomata This substance contains sugars, mainly saccharose permitting the transport of vital gasses (Lendzian, 2006). (Zimmermann & Milburn, 1975), but also many ions, It is these lenticels which are responsible for the porosity metabolites, RNAs, proteins and hormones (Dinant, of cork (Pereira 1996). 2008), transported from photosynthetic organs through all the living tissue. Sap is the essential energetic source for However, diffusion rates are related to lenti- the plant’s metabolism. In the goal to measure it, Helfter, cel density and size, which vary substantially among spe- Shephard, Martínez-vilalta, Mencuccini, & Hand (2017) cies. For example, in turkey cork oak, developed a non-invasive system allowing the direct de- the lenticular channels are rare and not required for gas tection of sap movements and velocity by a thermal meth- exchanges (Leite & Pereira, 2017; Şen, Miranda, Santos, od. Graça, & Pereira, 2010). The multiple functions of tree bark —4/7

The resistance to efflux may depend on bark thick- 4 Protective function of bark ness, but also to the degree to which bark tissues are im- pregnated with suberins, lignins and waxes (Lendzian, 2006). Suberins, which represent 53% of the cell wall of 4.1 Protective mechanisms and adapta- phellem can reduce the permeability of bark to water and tions of bark gases (Leite & Pereira, 2017; Pereira, 2015). Furthermore, the periderm at the surface of the bark can reduce water Many animals globally specialize in herbivory of evaporation and have a negative consequence on gas ex- trees (all parts, e.g. LIST), such as vertebrates and insects change between the tree and the atmosphere (Groh, (principally beetles (Tavakilian, Berkov, Meurer-Grimes, Hübner, & Lendzian, 2002). & Mori, 1997)), which significantly impact tree health (Paine et al., 2010). The bark is first to be impacted and thereby has an 3 Stem mechanical support important role to play in protecting the entire tree. More specifically, given that the cutinized epidermis or suber- The physiological function of the bark is important ized periderms of trees are the first tissues that potential to ensure nutrition of the tree and it allows to the tree to pathogens and predators encounter (Kolattukudy and synthesize its stems and leaves. The whole leaves and Koller 1983), and given that the majority of tree species stems form the canopy which is a massive and heavy can live for centuries, the protection bark is effective structure. Mechanical support is necessary to resist against (Biggs, 1992). rupture of its stems and trunk. Bark has an essential role in the mechanical support of the tree (C. Romero, 2013). Trees adapt to tolerate the kinds of pressures and damage to which they are habitually exposed. The adapta- The different proportions of bark thickness are ob- tions can be morphologic (such as spines (Campbell, served in old and young stems: more bark covers the trunk 1986; Cooper & Ginnett, 1998), metabolic (such as secre- at the tips and consequently less wood is produced in tions (Langenheim 2003), or toxic secondary compounds these areas (K J Niklas, 1999; Rosell et al., 2014). In (Coley, Bryant, & F. Stuart Chapin, 1985; Reichardt et al., young stems, bark stiffness is associated to bark thickness. 1990)), or behavioral (establishment of relationships with In the opposite of what can happen in the young stems, the herbivore-repelling ants (Janzen, 1973)) (from Romero & contribution of bark to mechanical support in later tree Bolker, 2008). development steadily decreases. In conclusion, it seems that the contribution of bark to branch stiffness is mainly Most pathogens are unable to directly penetrate the related to bark quality (Rosell et al., 2014). However, corky suberized tissues of most outer bark (such as phel- along the ontogeny, bark's contribution to mechanical lems which have 53% suberinised cell walls) and rhyti- support comes mostly from higher quantities of bark ra- dome. These outer layers represent defensive barriers to ther than tissue quality (Rosell et al., 2014). pathogen ingress (Biggs, 1992) and allow the inner tissues of the tree to be resistant to acid among other things (Leite Moreover, wood, of course, plays an important role & Pereira, 2017; Pereira, 2015). in mechanical support, and it is not clear if both bark and wood participate equally to this function (Karl J. Niklas, Another well studied bark function is protection 1992; Rosell et al., 2014). The contribution of wood may against fire damage. According to Brando, Nepstad, & surpass the one of bark in the mechanical support of the Balch (2012), bark resistance to fire damage can be under- tree (Rosell et al., 2014). stood according to two major parameters: the heat transfer rates (which is the reverse of cambium insulation) and the In the same time, particular environmental condi- density of bark and wood. These two parameters are influ- tions may lead to favor bark contribution in the mechani- enced by tree size, bark thickness and water storage. cal support. For example, in moister forest, where trees can be taller, the bark appears stiffer (Rosell et al., 2014). Moreover, phellem is very durable, it is flexible Or in the African Baobab, the secondary phloem occupies without fracturing under compression (Pereira, 2007). 75 % of the bark volume (Kotina & Oskolski, 2017). In This property is important to avoid trunk damage from these two cases, mechanical role of the bark is important, impacts such as from other trees. but it is not expressed in the same way. In the moist forest, rigidity of the bark is prioritized. In the dry forest, the important volume of the bark which is involved in 4.2 Bark self-repair mechanisms droughtness solutions, plays also an important role in the mechanical support. In contrast with leaves, tree stems need to persist Mechanical properties attributed to the bark are and recover after damage. The sensitivity to damage var- complex and difficult to understand. Further study should ies considerably among tree species. Once damaged, the clarify these previous results. rate at which bark grows to close the wound varies widely between trees (Claudia Romero & Bolker, 2008).

The multiple functions of tree bark —5/7

The ability of parenchyma cells to recover is linked some functions are expressed to their maximum capacity, to the capacity of cells surrounding wounds to become some functions are neglected, and some have a medium meristematic (Claudia Romero & Bolker, 2008; expression. The priority of the tree leads to these trade- Zimmerman & Brown, 1971). Rays also play a role in offs. Consequently, trade-offs and functional coordination wound phellogen healing (Miller and Barnett 1983). The are common in bark, and depend on environment condi- ability of bark to heal itself is often a trade-off between tions and constraints. speed and efficiency. For example, Chorisia speciosa In order to enhance our understanding of bark func- closes bark wounds rapidly, and this speed compensates tions and the variations observed in bark morphology and for partial inefficient decay control. By contrast, Pseu- physiology, we should adopt a systematic approach. The dolmedia laevis closes wounds slowly, but compensates study of one functional trait must be correlated with the with efficient defenses against decay. The relationship simultaneous study of other functions. Further study is between anatomical and/or structural traits and damage required which analyses one function in relation with response variables reveals that species with favorable several different functional traits. These overarching stud- traits for rapid wound closure (e.g., widely dilating rays) ies should enable us to have a better view of the trade-offs have traits that favor xylem decay spread (e.g., low wood made by trees in function of environmental pressure, her- density) (Claudia Romero & Bolker, 2008). bivory and other influencing factors. These kind of study, rarely made nowadays except by Rosell (Rosell, 2016; Rosell et al., 2013) could permit us to have a better under- Discussion and conclusion: standing about the influence of morphology and anatomy on the operation of, and the functions performed by, bark. trade-offs of functions in bark

We saw that bark has a complex internal structure, Acknowledgements with an important variability across species, reflecting the manifold functions of barks. The multiple functions we A particular thanks to Bruno Clair and Romain have mentioned are mostly studied using functional traits Lehnebach from the ―Laboratoire de Sciences du bois‖ in (barks functions being often more difficult to measure) Kourou for their contribution to this work. such as bark density or thickness which permit to describe the bark diversity observed about structure, morphology, anatomy and physiology. And this is with these traits that we try to explain the huge functional diversity of bark References (Rosell et al., 2013).

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Appendix

Table I - Several denominations of bark. The different names used in the document are listed in the first col- umn. The respective correspondences of these names with other English terms, but also with French terms are reviewed in the second and third column.