The Anatomical Basis of the Link Between Density And'mechanical
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CSIRO PUBLISHING Functional P lant Biology, 2013, 40, 400-408 http://dx.doi.org/10.1071/FP12204 The anatomical basis of the link between density and mechanical strength in mangrove branches Nadia S. SantiniA, Nele SchmitzB/C, Vicki BennionA and Catherine E. LovelockA/D AThe School of Biological Sciences, The University of Queensland, St Lucia, Qld 4072, Australia, laboratory for Plant Biology and Nature Management, Vrije Universiteit Brussel, Brussels 1 050, Belgium. cLaboratory for W ood Biology and Xylarium, Royal Museum for Central Africa, Leuvensesteenweg 1 3, 3080 Tervuren, Belgium. DCorresponding author. Email: [email protected] Abstract. Tree branches are important as they support the canopy, which controls photo synthetic carbon gain and determines ecological interactions such as competition with neighbours. Mangrove trees are subject to high wind speeds, strong tidal flows and waves that can damage their branches. The survival and establishment of mangroves partly depend on the structural and mechanical characteristics of their branches. In addition, mangroves are exposed to soils that vary in salinity. Highly saline conditions can increase the tension in the water column, imposing mechanical stresses on the xylem vessels. Here, we investigated how mechanical strength, assessed as the modulus of elasticity (MOE) and the modulus of rupture (MOR), and density relate to the anatomical characteristics of intact mangrove branches from southeast Queensland and whether the mechanical strength of branches varies among mangrove species. Mechanical strength was positively correlated with density of mangrove intact branches. Mechanical strength (MOE) varied among species, with Avicennia marina (Forssk.) Vierh. branches having the highest mechanical strength (2079 ± 176 MPa), and Rhizophora stylosa Griff, and Bruguiera gymnorrhiza (L.) Savigny ex Lam. and Poiret having the lowest mechanical strength (536.8 ± 39.2 MPa in R. stylosa and 554 ± 58.2 MPa in B. gymnorrhiza). High levels of mechanical strength were associated with reductions in xylem vessel lumen area, pith content and bark content, and positively associated with increases in fibre wall thickness. The associations between mechanical strength and anatomical characteristics in mangrove branches suggest trade-offs between mechanical strength and water supply, which are linked to tree growth and survival. Additional keywords:fibres, intact branches, modulus of elasticity, modulus of rupture, xylem vessels. Received 9 July 2012, accepted 17 November 2012, published online 11 January 2013 Introduction mechanical strength (Jacobsen et al. 2007; Chave et al. 2009). The wood of branches performs vital functions during the life of a The density of intact branches is not determined by the wood tree and also determines important ecosystem properties (Chave (xylem) characteristics only. The density of intact branches is also et al. 2009). Wood density is an important characteristic defining dependent on all the cell tissues that comprise the intact branch the mechanical properties of the wood and its performance, segment, such as the pith, composed of parenchyma, and the bark, such as resistance to breakage during high winds (Curran et al. composed of phellem, phloem and cambial cells (Sterck et al. 2008; Niklas and Spatz 2010) and susceptibility to insects and 2006; Onoda et al. 2010). pathogens (Augspurger and Kelly 1984). The wood density also The structure and function of the tissues that constitute the influences the physiological functions of branches because of different parts of a plant (i.e. main stems, branches androots) vary, wood's role in water transport (Prattet al. 2007). For instance, corresponding to the distinct hydraulic and mechanical demands high wood density has been found to decrease vessel implosion of these parts (Schweingruber et al. 2008). Studies of wood by reducing the mechanical stresses associated with the negative structure and function in plants have widely focussed on the pressure in the water column during drought (Hacke et al. 2001 ; wood of main stems because of its importance in forestry. Fewer Jacobsen et al. 2005). studies have addressed the relationship between the structure Wood density in branches is dependent on the anatomical and mechanical strength of intact branches (but see van Gelder characteristics of the wood such as xylem vessels and fibres et al. 2006; Sterck et al. 2006; Onoda et al. 2010), but intact (Jacobseni/al. 2005; Prestone/al. 2006). Inangiosperms, wood branches affect tree growth and survival. Branches are involved density has been observed to decline with decreasing vessel area in leaf deployment and expansion of canopies (e.g. when and thus the space for water transport (Prestonet al. 2006), and to competition for light with neighbouring trees occurs; e.g. increase with increasing fibre wall thickness, which provides Henriksson 2001). In addition, branches are more vulnerable Journal compilation © CSIRO 2013 www .publish. c siro. au/j oumals/fpb Mechanical strength in mangrove branches Functional Plant Biology 401 to wind stresses than main stems (Whigham et al. 1991; van positions that are higher in the intertidal zone. When rainfall Gelder et al. 2006). runoff is limited, soil pore water that is high in the intertidal zone Here, we studied the mechanical strength, density and becomes highly saline due to evaporation of the seawater. Highly anatomy of intact canopy branches (including the xylem, the saline conditions are conditions similar to drought and can result pith, and the bark) in mangroves from southeast Queensland. in an increase in the tension of the water column within the xylem; Mangroves in this study were selected to include species with this tension can impose mechanical stresses on the xylem vessels typical and atypical secondary growth. Typical secondary growth (Jacobsen et al. 2005). refers to a single cylindrical cambium that produces phloem In this work we assessed: (1) the relationship between externally and xylem internally, whereas atypical secondary mechanical strength, the density of intact branches and growth displays successive cambia (i.e. forming consecutive anatomy in mangroves; (2) whether the mechanical strength of bands of xylem and phloem; Schweingruber et al. 2008). branches varies among mangrove species, and (3) whether Species with typical secondary growth for this study were mechanical strength and the density of intact branches varies three members of the family Rhizophoraceae, Rhizophora betweenH. marina specimens from the high and the low intertidal stylosa Griff., Bruguiera gymnorrhiza (L.) Savigny ex Lam. zones. and Poiret, and Ceriops australis (C.T. White) Bailment T.J. Sm. and J.A. Stoddart; and Aegiceras corniculatum (L.) Blanco Materials and methods from the Myrsinaceae (Shi et al. 2005). In addition, the most widely distributed mangrove across the Indo-West Pacific shores, Site description and sample collection Avicennia marina (Forssk.) Vierh., exhibits atypical secondary Our study sites were located in southeast Queensland, where the growth. Including the pith and bark in this study was important mean air temperature is 21°C (a mean minimum temperature because (1) we were interested in the mechanical properties of of 15°C and a mean maximum temperature of 25°C) and the intact branches, not just the density or the mechanical strength of mean rainfall is 1150mmyear_1. Our study sites were in the the xylem tissue, and (2) species varied in their wood anatomy, Tinchi Tamba Wetlands Reserve (27.23°S, 153.02°E) and with the inclusion of phloem within the wood ofA. marina. the Point Halloran Reserve (27.56°S, 153.28°E), 35km to the Therefore, inclusion of the bark in other species provided an south of the Tinchi Tamba site. These sites were chosen because appropriate comparison. they contain five of the most abundant mangrove species in Mangroves grow on the coasts of tropical and subtropical southeast Queensland (Table 1). shores. Mangroves are subject to high wind speeds, strong tidal At each site and on the basis of elevation relative to mean sea flows and waves. In Queensland, wind gusts can reach 90 km IT1 level, we defined two intertidal zone habitats: low and high during thunderstorms and >200 km IT1 during cyclonic activity intertidal. We assessed the salinity of soil pore water at each (Australian Bureau of Meteorology 2012) and can cause intertidal zone from each site. We collected pore water samples at structural damage to branches of trees (e.g. Paling et al. 2008). 30 cm depth using a suction device (McKee et al. 1988) and Therefore, tree establishment and survival under different analysed them with a handheld refractometer (W/ATC 300011, environments partly depend on the structural and mechanical SPER Scientific, Scottsdale, AZ, USA). characteristics of their branches (van Gelder et al. 2006; Curran We collected canopy branches from each species in each et al. 2008). intertidal zone (low and high intertidal) during July 2010; see In addition to wind and wave forces, mangroves are exposed to sample sizes and details of collection dates in Table 1. We tested soils that vary in salinity. Mangrove trees that grow low in the for differences between species in mechanical strength (modulus intertidal area are more frequently inundated than trees growing in of elasticity (MOE) and modulus of rupture (MOR)) and the Table 1. Characteristics of the mangrove species from southeast Queensland, including growth form, position along the intertidal zone, pore water salinity and sample size The first collection was performed on 20 July 2010 and the second collection was performed on 30 July 2010. The samples from the first collection were used to measure the modulus of elasticity (MOE), modulus of rupture (MOR) and density of intact branches. The samples from the second collection were used to measure the MOE, MOR and density of intact branches, and xylem and branch characteristics, ppt, parts per thousand Site Species Growth Intertidal Salinity n First Second Total (n ) form zone (ppt)±s.e. collectionin) collectionin) Point Halloran Avicennia marina Tree Low 32 ±1 5 10 - 10 Bruguiera gymnorrhiza Tree 25 5 30 Rhizophora stylosa Tree 17 6 23 A.