ESTIMATING WATER IN LIVING WOODY STEMS - A REVIEW

ESTIMATIVA DE ÁGUA EM CAULE LENHOSOS VIVOS - UMA REVISÃO

ABSTRACT

Predicted climate changes due to greenhouse gas emissions will alter site and ecological conditions, increase instability in many ecosystems and expand the value of forest carbon and wood energy. Woody plants most often are faced with drought stresses, not only because of erratic rainfall, but also the result of climatic changes. Natural variability among wood species in terms of chances in induced water stress in stem moisture content is large. Under severe water deficit, plants have to face the dilemma of dying by drying or being starved of carbon. Changes in the water content of extensible tissues of the stem are readily reversible, causing diurnal variation driven by changing water potential in the xylem. This review intends: 1. to address how stems in woody species play an important role in water storage relevant to plant hydraulics, and 2. to present methodologies to estimate water content in stems of wood species.

Keywords:
Plant hydraulics; Non-destructive techniques; Electrical moisture measurements

RESUMO

Mudanças climáticas previstas alterarão o local e as condições ecológicas, aumentarão a instabilidade em muitos ecossistemas e expandirão o valor do carbono florestal e da energia da madeira. Plantas lenhosas na maioria das vezes são confrontadas com deficit hídrico, não só causado por chuvas irregulares, mas também resultante das mudanças climáticas. A variabilidade natural entre as espécies lenhosas em termos de mudanças induzidas pelo estresse hídrico no teor de umidade do tronco é grande. Sob deficit hídrico severo, as plantas enfrentam o dilema de morrer por falta de água ou de carbono. Mudanças no conteúdo de água dos tecidos elásticos do caule são facilmente reversíveis, causando variação diurna impulsionadas pela mudança do potencial de água no xilema . Esta revisão pretende abordar como caules de espécies lenhosas desempenham um papel importante no armazenamento de água relevante ao sistema hidráulico das plantas e apresentar metodologias atuais para estimar o teor de água no caule de espécies lenhosas.

Palavras chave:
Hidráulica de plantas; Técnicas não destrutivas; Medições elétricas da umidade

INTRODUCTION

Future trends of global climate indicate a worldwide increase in the risk of acute droughts and heat waves (ALLEN et al., 2010). Under the scenario of drought induced by climate change, an important concern in forestry is if intraspecific genetic resources available to tree species hold enough variability to cope with future climate change (ALBERTO et al., 2013).

Environmental biotic stresses have adverse effects on plant growth and productivity and it can also become more widespread in future decades. Therefore, rapid and sensitive quantification of stress in trees due to irrigation practices, drought, salinity, pollution, lack of nutrients or diseases should be considered as necessary research proposals (NADLER; TYREE, 2008).

Under severe water stress, terrestrial plants tend to close the stomata to avoid water loss. Prevention of hydraulic failure by stomatal closure results in carbon starvation by plants (HARTMANN, 2015). It is therefore commonplace to infer that an important imbalance between uptake and loss of either carbon or water would be responsible for plant death (ALLEN et al., 2010; McDOWELL, 2011; COCHARD; DELZON, 2013).

Therefore, accurate measurements of plant water status are essential for a better understanding of productivity and management practices of wood species under various present and future environmental conditions.

Variations in wood stem water content are generally related to seasonal rainfall. Size fluctuations of stem diameter are associated particularly with variation in the water content of the bark and sapwood swelling and contraction.

DROUGHT EFFECTS ON WOOD SPECIES

Forest mortality associated with climate-related events have been reported with increasing frequency in tropical rainforests (PHILLIPS et al., 2009), temperate mountainous and Mediterranean forests (CARNICER et al., 2011) and boreal forests (PENG et al., 2011). Both hydraulic failure and carbon starvation plant processes contribute to mortality according to current leading hypothesis (SEVANTO et al., 2014). Expected hydraulic failure occurs when water loss from transpiration is sufficiently greater than uptake by roots resulting in progressive cavitation and conductivity loss of the xylem. Carbon starvation is hypothesized to result from avoidance of hydraulic failure through stomatal closure causing negative carbon balance (McDOWELL et al., 2008).

When transpiration starts in the early morning tension is created in the xylem tissue originated from the evaporative surface of the leaves down to every organ of the plant. Part of the water stored in plant tissues during the night is then lost, allowing the plant to respond rapidly to changes in atmospheric demand without the need to rely on water uptake by the roots. This affects every water-storing organ of the plant (Figure 1) so diurnal diameter changes occur in all parts of the plant, including the stem, branches, roots, leaves, and fruits.

FIGURE 1
Two days of radial stem diameter measurements. (I) increment, (S) shrinkage, (R) recovery, and (E) expansion (after Drew and Downes, 2009).

Changes in the water content of extensible tissues of the stem are readily reversible, causing diurnal variation driven by changing water potential in the xylem. Water can be withdrawn from the inner woody tissues of the xylem but then cavitation rather than shrinkage occurs because this tissue is less elastic. The water stored in elastic tissues of the stem buffers the lag between roots and shoot preventing embolisms and ensuring optimal transpiration rates (PERAMAKI et al., 2005).

Drought-induced mortality would result from a non-mutually exclusive interaction of several mechanisms (NARDINI et al., 2013; SEVANTO et al., 2014). According to several authors (HARTMANN et al., 2013; URLI et al., 2013) events such as hydraulic failure, carbon starvation and biotic agent demographics are the most notorious mechanisms involved in mortality induced by drought.

Xylem tensions that cause 5 to 30 % loss of water transport capacity could generate a runaway embolism and lead to catastrophic xylem dysfunction that result in hydraulic failure. Plant carbon starvation is argued to be a consequence of avoiding hydraulic failure by means of stomatal closure. Drought drives changes in the demographics of biotic mortality agents resulting in tree mortality (PLAUT et al., 2012).

Recent work by Rowland and collaborators (2015) using data from a long-term experimental drought study at the Brazilian Amazon region concluded that tropical rainforests are likely to experience exceptional high mortality resulting from hydraulic processes rather than by gradual carbon starvation.

WATER FROM WOOD STEMS

The natural variability among wood species in terms of their water-stress-induced changes in stem moisture content is large. Plants have evolved different strategies in facing the potential risks of drought-induced hydraulic failure. Some species tend to take a conservative water-use strategy, while others are inclined to exhibit an adventurous strategy for more prodigal water use and high growth rates (HAO et al., 2010, 2013). The physiological responses of plants to water deficit and their relative importance for crop productivity vary with species, soil type, nutrients and climate.

Presence of a woody stem is a key feature that differentiates woody plants from herbaceous plants. Zweifel et al. (2001) reported that in young Picea abies L. trees the percentage of available water from the respective total tissue water reserves was up to 25 and 6% for crown and stem, respectively. Stem traits emerge as important plant functional traits because of their role for stability, defense, architecture, hydraulics, carbon gain and growth potential (CHAVE et al., 2009).

In angiosperm tree species, wood or xylem is composed of three types of tissues that fulfill different functions. The extent in which wood plant species can conduct water and resist xylem cavitation in the stem is determined by vessel adaptation. Failure of the conductive tissue to resist high negative pressures can result in collapse of the conduit walls resulting in cavitation.

Species with high wood density have xylem conduits less susceptible to cavitation and embolism during the dry season (MEINZER et al., 2009) as well as tend to accumulate less water than those with low-density wood (OSUNKOYA et al., 2007). Less porous wood shows more space filled with cell walls composed by cellulose, hemicellulose and lignin. As a result, less water is stored within the stem wood (McCULLOH et al., 2011). Dias and Marrenco (2016) reported a negative correlation between wood water content and wood density in 28 tree species from a terra-firme rain forest in central Amazonia.

Water deficit measured in terms of water potential has a direct impact on plant performance. As water potential declines, plant growth and gas exchange followed by yield and finally survival are impacted as water potential progressively decreases. Under severe drought stress, plants may experience severe hydraulic failure or even diebacks (ANDEREGG et al., 2013).

Water is transported from the roots to the leaves through the xylem of woody plants under negative pressure (TYREE, 1997). One important aspect of stems in woody species is that of water storage (HOLBROOK, 1995). The water content of stems varies as xylem water potential increases and decreases, respectively. Therefore, a non-destructive method to measure stem water content (θstem) = (volume of water) ÷ (volume of stem) could be useful in monitoring the drought stress status of plants.

DESTRUCTIVE METHODOLOGY

The simplest technique of measuring stem water content (θstem) sometimes referred as stem relative water content (RWCstem) is to collect stem cores and directly measure the water content by weighing tissue samples before and after drying (CLARK and GIBBS, 1957). Such traditional gravimetric measurement is labor intensive, difficult to automate and harmful for the tree after repeated sampling (LÓPEZ-BERNAL et al., 2012).

Gravimetric determination of θstem is simple and does not require expensive equipment. It involves obtaining measurements of fresh weight, turgid weight, and dry weight made on the same sample. It is calculated by [(W-DW) / (TW-DW)] x 100, where W is the sample fresh weight, TW is the sample turgid weight and DW is the sample dry weight.

NONDESTRUCTIVE METHODOLOGIES

Stem water content (θstem) of terrestrial plants has been measured in situ using various sensor techniques.

Stem psychrometers are used to record plant water potential of living plants without damaging them. The stem psychrometer is attached to stem with diameters up to 5.5 cm by clamps using light pressure. Measurement can be either psychometric (wet bulb thermometer measurement) or hygrometric (measurement of dew point) resulting in precise and reproducible measurement of the plant water potential (VOGT, 2001).

More recent instruments are gamma-ray densitometry (EDWARDS; JARVIS, 1983; BROUGH et al., 1986), magnetic resonance imaging (REINDERS et al., 1988; WINDT et al., 2009; CHOAT et al., 2010; SCHEPPER et al., 2012), x-ray computer tomography (RASCHI et al., 1995), stem diameter transduction (FERNANDEZ; CUEVAS, 2010), time domain reflectometry (CONSTANTZ; MURPHY, 1990; HOLBROOK et al., 1992; IRVINE; GRACE, 1997; WULLSCHLEGER et al., 1998; SPARKS et al., 2001), compensate heat pulse (SWANSON, 1962) and frequency-domain (FD) capacitance (HOLBROOK et al., 1992; KUMAGAI et al., 2009; HAO et al., 2013).

Among the techniques above listed, gamma ray instruments are highly accurate and noninvasive (BROUGH et al., 1986; JONES, 2004) but carry a potential risk of radiation exposure restricting their application (IRVINE; GRACE, 1997).

The magnetic resonance imaging (MRI) method is also noninvasive and safe, but it is costly and impractical for long-term monitoring of plant water status in natural conditions. The imaging branch of nuclear magnetic resonance (NMR), namely MRI can estimate in vivo the amount of water in tree stems and allows differentiation between different stem tissues (WINDT et al., 2009). For example, Schepper et al. (2012) evaluated the relationship between MRI and trunk diameter variations in 2 year-old Quercus robur L. with a stem diameter of 1.4 ± 0.1 cm and a height of 112 ± 3 cm. The authors reported a strong correlation between transpiration-induced changes in stem diameter and the amount of stem water, demonstrating the value of stem diameter variations for estimation the in vivo use of internally stored water.

Different types of sensors for measuring stem diameter variation (SDV) have been used to provide information about water storage because the diurnal recharge and discharge of water in stems causes stem tissue to swell and shrink. However, interpretation of SDV values are not straightforward especially when plants grow under different degrees of drought stress, as pointed out by Fernandez and Cuevas (2010). Additionally, SDV is modulated by plant age, measured position on the stem and the irreversible change of stem diameter caused by plant growth.

The compensate heat pulse method (CPH) is based on the measurement of the temperature difference between sensors located above and below a heater inserted in the tree trunk. CHP has been widely used to determine the dynamics of transpiration by measuring sap flow in conductive organs of woody plants (SWANSON; WHITFIELD, 1981) and presents a great potential for irrigation scheduling (FERNÁNDEZ et al., 2008). On the other hand, the method assumes that wood acts as an isotropic medium, which is unrealistic and may slightly affect the accuracy of the technique.

Time domain reflectometry (TDR) and heat field deformation (HFD) sensors are invasive techniques because both depend on inserting two or more waveguide lines into the stem, causing some tissue damage in the stem. The damaged tissue response to the probe insertion could last a few of weeks until the sensor signal becomes ‘normal’ (WULLSCHLEGER et al., 1998; LU et al., 2002; NADLER et al., 2003). Compared to other techniques, TDR is safe, quick, non-destructive and simple to use allowing easy replication in the field. An advantage of HFD sensors compared to TDR sensors is that the geometry of HFD probes can be very adaptable, facilitating development of a variety of configurations (SUN et al., 2005).

TDR appears to be a suitable candidate for routine monitoring of water content of tree stems for being relatively free of ground interferences and automatable and to follow diurnal changes in the water status of a tree trunk. However, because the dielectric constant of water (ε ≈ 80) is larger than that of other soil constituents (ε_air = 1, εsolids = 2-5), any change in the bulk dielectric of a composite material containing water, soil and air reflects a change in water content. Therefore, an empirical relationship (i.e. calibration equations) is estimated and used to convert TDR measurements of ε into volumetric water content (L.L^-1) values.

Three sources of experimental error have already been identified with TDR use (NADLER et al., 2003). Operator error described as technical error obtained when measuring volumetric water content by the same TDR probe because of poor probe installation or air gaps around the TDR rods. A systematic error in the measurements arising from the temperature influence on the coaxial cable dielectric length and an experimental error due to radial variability of stem morphology.

Trunk dendrometers have been widely assessed in fruit trees to monitor plant water status (ORTUÑO et al., 2010). When transpiration (Ep) begins early in the morning, a tension is created in the xylem from the evaporative surface of the leaves to every organ of the plant. In large plants such as woody species, the water stored within the trunk may contribute substantially to Ep (CERMÁK et al., 2007). Water from the phloem and related tissues such as cambium and green bark as well as from living tissues of the outer xylem (ZWEIFEL et al., 2000) is withdrawn and lost by Ep resulting in a reduction of trunk diameter.

Depending on the dendrometer model and the purpose of the measurement, nails or screws may have to be driven into the trunk either to support the instrument or to serve as a fixed reference. This disturbance frequently results in abnormal growth acceleration at the vicinity of the injury. Therefore, the dendrometer holder is usually attached tightly to the trunk by elastic straps.

Dendrometers are installed on the side of the trunk opposite to the sun’s trajectory, to minimize negative effects of heating by direct solar radiation. In addition, dendrometers should be placed distant from the ground to avoid interference from growing weeds, and as far as possible from any trunk scars.

Two indexes of trunk diameter variations (TDV) from dendrometer records are normally calculated namely the maximum diurnal trunk shrinkage (MDS) and the trunk growth rate (TGR). MDS has the potential to serve as plant water stress indicator (FERNÁNDEZ; CUEVAS, 2010) because MDS is normally higher in plants with soil water deficit than in well-irrigated trees. In several woody species such as citrus (ORTUÑO et al., 2004), peach (MARSAL et al., 2002), apple (DOLTRA et al., 2007), plum (INTRIGLIOLO; CASTEL, 2006), almond (GOLDHAMER; FERERES, 2001), pomegranate (INTRIGLIOLO et al., 2011) and persimmon Kaki (BADAL et al., 2010). MDS was described to be a reliable indicator while in others such as olive (MORIANA; FERERES, 2002) and grapes (INTRIGLIOLO; CASTEL, 2007) it was not useful.

In spite of the accuracy of the above described techniques, there are still opportunities for development of a method with a straightforward and less expensive alternative, such as electrical resistance that may be practical, easy to use and economical. Hand-held moisture meters provide a rapid method for obtaining the moisture content of wood and wood products during processing. Hand-held moisture meters measure electrical properties that correlate with the amount of water in the wood (GILLIS et al., 2001). Types of moisture meters available in the market are either resistance-type or dielectric-type moisture meters.

Generally, in porous materials and solutions, electrical conductivity (σ) is linearly related to the product of the volume and ion concentration (NADLER, 2005). However, in stems, bulk stem electrical conductivity (σ stem) is far more sensitive to changes in volumetric water content (θ) than to changes in sap ionic concentration (NADLER et al., 2006).

Variations in electric resistance have been used to measure water content of soils and cut timber (SKAAR, 1988) and to detect decaying wood in trees (SHIGO; SHORTLE, 1985). In wood stems, the resistance to low frequency alternating current (i.e. impedance) depends mainly on the ion content and quantity of cell sap released into the apoplast by living cells wounded during insertion of the electrodes. Resistance varies with the fraction of living cells in the bark and sapwood of a stem and with the water status of these tissues (BLANCHARD et al., 1983).

Borchert (1994) reported stem water content measured as electric resistance between nails driven 20 mm deep into tree trunks of more than 30 species from Costa Rica correlated with wood density and saturation water content measured with a pressure chamber.

FINAL CONSIDERATIONS

Water availability influences the distribution, structure and composition of terrestrial plant communities. At the same time, plants are a major conduit for water to return to the atmosphere, and hence influence climate and exert strong effects on hydrologic fluxes in the land-atmosphere system.

Terrestrial plants have mechanisms of internal water flux regulation, which uncouple plant water status from atmospheric, and soil hydrological control linked to morphological and physiological traits (ZWEIFEL et al., 2002).

Stems and trunk have functional role of internal water storage in wood forest species. Therefore, it is likely that the functional importance of internal water storage in trees will increase to insure fast establishment and survival of tree seedlings through artificial regeneration especially under future scenario of climate change.

Nondestructive monitoring of water content in living trees and seedlings offers opportunities for development of sensors and technologies suitable for irrigation, real-time detection of plant water stress and for studies of water use mechanisms in trees and storage ability of wood stems.

REFERENCES

• ALBERTO, F. J.; AITKEN S.; ALÍA, R. Potential for evolutionary responses to climate change-evidence from tree populations. Global Change Biology, v.19, p.1645-1661, 2013.
• ALLEN, C.D.; MACALADY, A.K.; CHENCHOUNI, H.; BACHELET, D.; McDOWELL, N.A. Global overview of drought and heat-induced tree mortality reveals emerging climate change risks for forests. Forest Ecology and Management, v. 259, p.660-684, 2010.
• ANDEREGG, W.R.L.; KANE, J.M.; ANDEREGG, L. Consequences of widespread tree mortality triggered by drought and temperature stress. Nature Climate Change, v.3, p.30-36, 2013.
• BADAL, E.; BUESA, I.; GUERRA, D.; BONET, L.; FERRER, P.; INTRIGLIOLO, D.S. Maximum diurnal trunk shrinkage is a sensitive indicator of plant water, stress in Diospyros kaki (Persimmon) trees. Agricultural Water Management, v.98, p.143-147, 2010.
• BLANCHARD, R.O.; SHORTLE, W.C.; DAVIS, W. Mechanism relating cambial electrical resistance to periodic growth rate of balsam fir. Canadian Journal of Forest Research, v.13, p.472-480, 1983.
• BORCHERT, R. Electric resistance as a measure of tree water status during seasonal drought in a tropical dry forest in Costa Rica. Tree Physiology, v.14, p.299-312, 1994.
• BROUGH, D.W.; JONES, G.; BRACE, J. Diurnal changes in water content of the stems of apple trees, as influenced by irrigation. Plant Cell & Environment, v.9, p.1-7, 1986.
• CARNICER, J.; COLL, M.; NINVEROLA, M.; PONS, X.; SÁNCHEZ, G.; PEÑUELAS, J. Widespread crown condition decline, food web disruption, and amplified tree mortality with increased climate change-type drought. Proceedings of the National Academy of Sciences of the United States of America, v.10, p.1474-1478, 2011.
• CERMÁK, J.; KUCERA, J.; BAURERLE, W.L.; PHILLIP, N.; HINCKLEY, M. Tree water storage and its diurnal dynamics related to sap flow and changes in stem volume in old-growth Douglas-fir trees. Tree Physiology , v.27, p.181-198, 2007.
• CHAVE, J.; COOMES, D.; JANSEN, S.; LEWIS, S.L.; SWENSON, N.G.; ZANNE, A.E. Towards a worldwide wood economics spectrum. Ecology Letters, v.12, p.351-366, 2009.
• CHOAT, B.; MATTHEWS, M.A.; SHACKEL, K.A.; WADA, H.; McELRONE, A.J. Measurement of vulnerability to water stress-induced cavitation in grapevine: a comparison of four techniques applied to a long-vesseled species. Plant Cell & Environment , v.33, p.1502-1512, 2010.
• CLARK, J; GIBBS, R.B. Studies in Tree Physiology IV: Further investigations of seasonal changes in moisture content of certain Canadian forest trees. Canadian Journal of Botany, v.35, p.219-253, 1957.
• COCHARD, H.; DELZON, S. Hydraulic failure and repair are not routine in trees. Annals of Forest Science, v.70, p.659-661, 2013.
• CONSTANTZ, J.; MURPHY, F. Monitoring storage moisture in trees using time domain reflectometry. Journal of Hydrology, v.119, p.31-42, 1990.
• DIAS, D.P.; MARENCO, R.A. Tree growth, wood and bark water content of 28 Amazonian tree species in response to variations in rainfall and wood density. Journal of Biogeosciences and Forestry, v.9, p.445-451, 2016.
• DOLTRA, J.; ONCINS, J.A.; BONANY, J.; COHEN. M. Evaluation of plant-based water status indicators in mature apple trees under field conditions. Irrigation Science, v.25, p.351-359, 2007.
• DREW, D.; DOWNES, G.M. The use of precision dendrometers in research on daily stem size and wood property variation: A Review. Dendrochronologia, v.27, p.159-172, 2009.
• EDWARDS, W.R.N.; JARVIS, P.G. A method for measuring radial differences in water content of intact tree stems by attenuation of gamma radiation. Plant, Cell & Environment, v.6, p.255-260, 1983.
• FERNANDEZ, J.E.; CUEVAS, M.V. Irrigation scheduling from stem diameter variations: a review. Agricultural and Forest Meteorology, v.150, p.135-151, 2010.
• FERNANDEZ, J.E.; GREEN, S.R.; CASPARI, H.W.; DIAZ-ESPEJO, A.; CUEVAS, M.V. The use of sap flow measurements for scheduling irrigation in olive, apple and Asian pear trees and in grapevines. Plant Soil, v.305, p.91-104, 2008.
• GILLIS, C.M.; STEPHENS; W.C.; PERALTA, P.N. Moisture meter correction factors for four Brazilian wood species. Forest Products Journal, v.5, p.83-86, 2001.
• GOLDHAMER, D.A.; FERERES, E. Irrigation scheduling protocols using continuously recorded trunk diameter measurements. Irrigation Science , v.20, p.115-125, 2001.
• HAO, G.Y.; SACK, L.; WANG, A.Y.; CAO, K.F.; GOLDSTEIN, G. Differentiation of leaf water flux and drought tolerance traits in hemiepiphytic and nonhemiepiphytic Ficus tree species. Functional Ecology, v.24, p.731-740, 2010.
• HAO, G.Y.; WHEELER, J.K.; HOLBROOK, N.M.; GOLDSTEIN, G. Investigating xylem embolism formation, refilling and water storage in tree trunks using frequency domain reflectometry. Journal of Experimental Botany, v.64, p. 2321-2332, 2013.
• HARTMANN, H. Carbon starvation during drought-induced tree mortality - are we chasing a myth? Journal of Plant Hydraulics, v.2, p. 1-5, 2015.
• HARTMANN, H.; ZIEGLER, W.; KOLLE, O.; TRUMBORE, S. Thirst beats hunger - declining hydration during drought prevents carbon starvation in Norway spruce saplings. New Phytologist, v.200, p.340-349, 2013.
• HOLBROOK, N.M. Stem water storage. In: Plant Stems: Physiology and Functional Morphology. Ed. B.L. Gartner. Academic Press, San Diego, 1995, p.151-174.
• HOLBROOK, N.M.; BURNS, M.J.; SINCLAIR, T.R. Frequency and time-domain dielectric measurements of stem water content in the arborescent palm Sabal palmetto. Journal of Experimental Botany , v.43, p.111-119, 1992.
• INTRIGLIOLO, D.S.; CASTEL, J.R. Usefulness of diurnal trunk shrinkage as a water stress indicator in plum trees. Tree Physiology , v.26, p.303-311, 2006.
• INTRIGLIOLO, D.S.; CASTEL, J.R. Evaluation of grapevine water status from trunk diameter variations. Irrigation Science , v.26, p. 49-59, 2007.
• INTRIGLIOLO, D.S.; PUERTOB, H.; BONETC, L.; ALARCÓND, J.J.; NICOLASD, E.; BARTUALE, J. Usefulness of trunk diameter variations as continuous water stress indicators of pomegranate (Punica granatum) trees. Agricultural Water Management , v.98, p.1462-1468, 2011.
• IRVINE, J; GRACE, J. Non-destructive measurement of stem water content by time domain reflectometry using short probes. Journal of Experimental Botany , v.48, p. 813-818, 1997.
• JONES, H.G. Irrigation scheduling: advantages and pitfalls of plant-based methods. Journal of Experimental Botany , v.55, p. 2427-2436, 2004.
• KUMAGAI, T.O.; AOKI, S.; OTSUKI, K.; UTSUMI, Y. Impact of stem water storage on diurnal estimates of whole-tree transpiration and canopy conductance from sap flow measurements in Japanese cedar and Japanese cypress trees. Hydrological Processes, v.23, p.2335-2344, 2009.
• LÓPEZ-BERNAL, A.; TESTI, L.; VILLALOBOS, F.J. Using the compensated heat pulse method to monitor trends in stem water content in standing trees. Tree Physiology , v.32, p.1420-1429, 2012.
• LU, P.; WOO, K.; LIU, Z. Estimation of whole-plant transpiration of bananas using sap flow measurements. Journal of Experimental Botany , v.53, p.1771-1779, 2002.
• MARSAL, J.; GELLY, M.; MATA, M; RABONES, J.; RUFAT, J.; GIRONA, J. Phenology and drought affects the relationship between daily trunk shrinkage and midday stem water potential of peach trees. Journal of Horticultural Science and Biotechnology, v.77, p.411-417, 2002.
• MCCULLOH, K.A.; MEIZER, F.C.; SPERRY, J.S.; LACHENBRUCH, B.; VOELKER, S.L.; WOODRUFF, D.R.; DOMEC, J-C. Comparative hydraulic architecture of tropical tree species representing a range of successional stages and wood density. Oecologia, v.167, p.27-37, 2011.
• MCDOWELL, N.G. Mechanisms linking drought, hydraulics, carbon metabolism, and vegetation mortality. Plant Physiology, v.155, p.1051-1059, 2011.
• MCDOWELL, N.; POCKMAN, W.T.; ALLEN, C.D. Mechanisms of plant survival and mortality during drought: why do some plants survive while others succumb to drought? New Phytologist , v.178, p.719-739, 2008.
• MEINZER, F.C.; JOHNSON, D.M.; LACHENBRUCH, B.; McCULLOH, K.A.; WOODRUFF, D.R. Xylem hydraulic safety margins in woody plants: coordination of stomatal control of xylem tension with hydraulic capacitance. Functional Ecology , v.23, p.922-930, 2009.
• MORIANA, A.; FERERES, E. Plant indicators for scheduling irrigation of young olive trees. Irrigation Science , v.21, p.83-90, 2002.
• NADLER, A. Methodologies and the practical aspects of the bulk soil EC (σa)-soil solution EC (σw) relations. Advances in Agronomy, v.88, p.274-308, 2005.
• NADLER, A.; RAVEH, E.; YERMIYAHU, U.; GREEN, S.R. Evaluation of TDR use to monitor water content in stem of lemon trees and soil and their response to water stress. Soil Science Society of America Journal, v.67, p.437-448, 2003.
• NADLER, A.; RAVEH, E.; YERMIYAHU, U.; GREEN, S.R. Stress induced water content variations in mango stem by time domain reflectometry. Soil Science Society of America Journal , v.70, p.510-520, 2006.
• NADLER, A.; TYREE, M.T. Substituting stem’s water content by electrical conductivity for monitoring water status changes. Soil Science Society of America Journal , v.72, p.106-113, 2008.
• NARDINI, A.; BATTISTUZZO, M.; SAVI, T. Shoot desiccation and hydraulic failure in temperate woody angiosperms during an extreme summer drought woody angiosperms. New Phytologist , v.200, p.322-329, 2013.
• ORTUÑO, M.F.; ALARCÓN J.J.; NICOLÁS, E.; TORRECILLAS, A. Comparison of continuously recorded plant-based water stress indicators for young lemon trees. Plant and Soil, v.267, p.263-270, 2004.
• ORTUÑO, M.F.; CONEJERO, W.; MORENO, F.; MORIANA, A.; INTRIGLIOLO, D.S.; BIEL, C.; MELLISHO, C.D.; PÉREZ-PASTOR, A.; DOMINGO, R.; RUIZ-SÁNCHEZ, M.C.; CASADESUS, J.; BONANY, J.; TORRECILLAS, A. Could trunk diameter sensors be used in woody crops for irrigation scheduling? A review of current knowledge and future perspectives. Agricultural Water Management , v.97, p.1-11, 2010.
• OSUNKOYA, O.O.; SHENG, T.K.; MAHMUD, N-A.; DAMIT, N. Variation in wood density, wood water content, stem growth and mortality among twenty-seven tree species in a tropical rainforest on Borneo Island. Austral Ecology, v.32, p.191-201, 2007.
• PENG, C.; MA, Z.; LEI, X. A drought-induced pervasive increase in tree mortality across Canada’s boreal forests. Nature Climate Change , v.1, p.467-471, 2011.
• PHILLIPS, O.L.; ARAGÃO, L.E.O.; LEWIS, S.L. Drought sensitivity of the Amazon rainforest. Science, v.323, p.1344-1347, 2009.
• PERAMAKI, M.; VESALA, T.; NIKINMAA, E. Modeling the dynamics of pressure propagation and diameter variation in tree sapwood. Tree Physiology , v.25, p.1091-1099, 2005.
• PLAUT, J.A.; YEPEZ, E.A.; HILL, J. Hydraulic limits preceding mortality in a pinon-juniper woodland under experimental drought. Plant, Cell & Environment , v.35, p.1601-1617, 2012.
• RASCHI, A.; TOGNETTI, R.; RIDDER, H.W.; BERES, C. Water in the stems of sessile oak (Quercus petraea) assessed by computer tomography with concurrent measurements of sap velocity and ultrasound emission. Plant, Cell & Environment , v.18, p.545-554, 1995.
• REINDERS, J.E.A.; VANAS, H.; SCHAAFSMA, T.J.; SHERIFF, D.W. Water balance in Cucumis plants measured by nuclear magnetic-resonance. Journal of Experimental Botany , v.39, p.1211-1220, 1988.
• ROWLAND, L.; da COSTA, A.C.L.; GALBRAITH, D.R. Death from drought in tropical forests is triggered by hydraulics not carbon starvation. Nature, v. 528, p.119-122, 2015.
• SCHEPPER, V.D.; DUSSCHOTEN, D.V.; COPINI, P.; JAHNKE, S.; STEPPE, K. MRI links stem water content to stem diameter variations in transpiring trees. Journal of Experimental Botany , v.63, p.2645-2653, 2012.
• SEVANTO, S.; McDOWELL, N.G.L.; DICKMAN, L.T.; PANGLE, R.; POCKMAN, W.T. How do trees die? A test of the hydraulic failure and carbon starvation hypotheses. Plant, Cell & Environment , v.37, p.153-161, 2014.
• SHIGO, A.I.; SHORTLE, W.C. Spruce budworms handbook. Shigometry: A reference guide. USDA Forest Service, Agriculture Handbook No. 646, 1985; 48 p.
• SKAAR, C. Wood-water relations. Springer-Verlag, Berlin. 1988. 283p.
• SPARKS, J.P.; GAYLON, S; CAMPBELL, R.; BLACK, A. Water content, hydraulic conductivity, and ice formation in winter stems of Pinus contorta: a TDR case study. Oecologia , v.127, p.468-475, 2001.
• SUN, Y.; MA, D.; LIN, J.; SCHULZE LAMMER, P.; DAMEROW, L. An improved frequency domain technique for determining soil water content. Pedosphere, v.15, p.805-812, 2005.
• SWANSON, R.H. An instrument for detecting sap movement in woody plants. U.S.D.A. Forest Service, Rocky Mountain Forest Range Experiment Station paper no. 68, 1962.
• SWANSON, R.H.; WHITFIELD, W.A. A numerical analysis of heat pulse velocity. Theory and practice. Journal of Experimental Botany , v.32, p.221-239, 1981.
• TYREE, M.T. The Cohesion-Tension theory of sap ascent: current controversies. Journal of Experimental Botany , v.48, p.1753-1765, 1997.
• URLI, M.; PORTE, A.J.; COCHARD, H.; GUENGANT, Y.; BURLETT, R.; DELZON, S. Xylem embolism threshold for catastrophic hydraulic failure in angiosperm trees. Tree Physiology , v.33, p.672-683, 2013.
• VOGT, U.K. Hydraulic vulnerability, vessel refilling, and seasonal courses of stem water potential of Sorbus aucuparia L. and Sambucus nigra L. Journal of Experimental Botany , v.52, p.1527-1536, 2001.
• WINDT, C.W.; GERKEMA, E.; Van AS, H. Most water in the tomato truss is imported through the xylem, not the phloem: a nuclear magnetic resonance flow imaging study. Plant Physiology , v.151, p.830-842, 2009.
• WULLSCHLEGER, S.D.; MEINZER, I.F.C.; VERTESSY, R.A. A review of whole-plant water use studies in trees. Tree Physiology , v.18, p.499-512, 1998.
• ZWEIFEL, R.; ITEM, H.; HÃSLER, R. Stem radius changes and their relation to stored water in stems of young Norway spruce trees. Trees, v.15, p.50-75, 2000.
• ZWEIFEL, R.; ITEM, H.; HÃSLER, R. Link between diurnal stem radius changes and tree water relations. Tree Physiology , v.21, p.869-877, 2001.
• ZWEIFEl, R.; BÖHM, J.P.; HÄSLER, R. Midday stomatal closure in Norway spruce-reactions in the upper and lower crown. Tree Physiology , v.22, p.1125-1136, 2002.

Publication Dates

• Publication in this collection
  Oct-Dec 2016

History

• Received
  28 Apr 2016
• Accepted
  25 Nov 2016