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Structure and Development |
2Estación Experimental La Mayora (CSIC) Algarrobo-Costa, E-29750 Málaga, Spain; 3Grupo de Caracterización y Síntesis de Biopolímeros Vegetales, Departamento de Biología Molecular y Bioquímica, Universidad de Málaga, E-29071 Málaga, Spain
Received for publication June 29, 2004. Accepted for publication December 13, 2004.
ABSTRACT
The mechanical properties of enzymatically isolated cuticular membrane (CM) from ripe tomato fruits were investigated at 10 to 45°C and relative humidity (RH) of 40 to wet. CM samples were stressed by uniaxial tension loads to determine their tensile modulus, E, breaking stress (strength), 
max, and maximum elongation, 
max. The CM stress–strain curves revealed a biphasic behavior when tested at RH values below wet conditions. In the first phase, CM responded to the loads by instantaneous extension with no further extension recorded until a further load was added: defined as pure elastic strain (Ee). In the second phase, CM responded by instantaneous extension and by some additional time-dependent extension, defined as viscoelastic strain (Ev). When CMs were submerged in aqueous solution (wet), the stress–strain curves were monophasic, with both elastic and viscoelastic strain. Ee depended on RH and was higher than Ev, which was independent of RH. Temperature decreased Ee and max of tomato fruit CM. Temperature response was not linear but consisted of two temperature-independent phases separated by a transition temperature. This transition zone has been related previously to the presence of a secondary phase transition in the cutin matrix of the tomato fruit CM.
Key Words: biphasic behavior • cuticular membrane • fruit cracking • Lycopersicon esculentum • plant biomechanics • tomato fruit
Most epidermal cells of the aerial parts of higher plants (such as leaves, fruits, and nonwoody stems), as well as some bryophytes, are covered by a continuous extracellular membrane of soluble and polymerized lipids called the cuticle or cuticular membrane (CM). The structure and composition of the CM varies among plants, organs, and growth stages (Kerstiens, 1996
), but it is basically composed of a cutin matrix with waxes embedded in (intracuticular) and deposited on the surface (epicuticular) of the matrix. Cuticular wax is a general term used to describe complex mixtures of homologous series of long chain aliphatics such as alkanes, alcohols, aldehydes, fatty acids, and esters, with the addition of variable proportions of cyclic compounds such as triterpenoids and hydroxycinnamic acid derivatives. The cutin consists largely of esterified fatty acids, with chain lengths mostly of 16 and 18 atoms of carbon, hydroxylated and epoxy-hydroxylated (Kolattukudy, 2001
; Heredia, 2003
).
A suite of physical, chemical, mechanical, and morphological properties gives the plant CM the characteristics of a unique and complex biopolymer. Since vascular plants managed to establish themselves on dry land around 400 million years ago, they have been protected by this complex biopolymer. From a physiological point of view, the main function ascribed to the CM is to minimize water loss (Riederer and Schreiber, 2001
). However, from a more general point of view, this role in the regulation of plant water loss is accompanied by other important functions: the CM limits the loss of substances from plant internal tissues, protects the plant against physical, chemical, and biological attacks and protects the fruits against the external environment both while the fruit is on the plant and after harvest. The CM enlarges as plant organs grow and, especially in fruits such as tomato that are without stomata, the main function of the CM is to maintain the integrity of the fruit (Wiedemann and Neihuis, 1998
). The cuticular membrane in association with the epidermis and subepidermis (the skin) is the morphological structure that confers the main mechanical strength to ripe tomato fruit; the skin is where failure (cracks) in the fruit are initiated because the skin surrounds a mass of more deformable material (Desmet, 2003
; Matas, 2004a
). Cuticular cracking is a persistent and widespread problem in some greenhouse-grown fruits such as tomatoes and peppers. Cracking appears mainly in ripe fruits, degrading fruit appearance and, subsequently, causing serious economic losses (Young, 1947
; Aloni, 1998
). Hence, the biomechanics of the skin and the CM are of great commercial importance.
The biomechanics of CM isolated from leaves of some species and from tomato (Lycopersicon esculentum Mill.) fruit were studied in some detail by Wiedemann and Neinhuis (1998)
, who demonstrated that mechanical characteristics of isolated CM vary greatly between species and, importantly for the tomato fruit, that the CM provides structural support for those fruits without hard internal tissue.
A number of tests have been performed to assess the mechanical properties of the skin in relation to fruit growth and cracking. Most tests used (puncture, bursting, and flat-plate compression) have many limitations because they generate a combination of compression, shear, and tensile stresses (Miles et al., 1969
; Voisey et al., 1970
). A few tensile tests have been performed in order to characterize the tensile properties of fruit skins of some species: tomato (Batal, 1970
; Murase and Merva, 1977
; Thompson, 2001
), onion (Allium cepa L.) (Hole, 2000
), and olive (Olea europaea L.) (Georget, 2001
). According to Hershko (1994)
, the tensile properties of ripe tomato skin can be described by a few values, namely strength (breaking strength), strain at failure, and stiffness, all of which can be determined by tensile tests. Tensile stress is usually plotted against the resulting strains to produce a graph called a stress– strain diagram. The slope of the initial linear region on the stress–strain diagram is called the elastic modulus, E, and provides an estimation of the stiffness. Strength can be defined as the maximum stress required to cause a material to break (Niklas, 1992
).
From stress–strain studies, the CM was described as a viscoelastic polymer network; isolated tomato fruit CM expands and becomes more elastic and susceptible to fracture after hydration, suggesting that water plasticizes the CM (Petracek and Bukovac, 1995
; Wiedemann and Neihuis, 1998
). This hypothesis was demonstrated by Round et al. (2000)
who, using atomic force microscopy and solid-state nuclear magnetic resonance, showed that water absorbed by the tomato fruit cutin acts as a plasticizer, promoting molecular flexibility and softening the polymer network. Those results agree well with the correlation between the occurrence of fruit cracking and the presence of high humidity or large application of water for several species such as tomatoes, sweet cherries and bell pepper (Peet, 1992
; Seske, 1995
; Aloni, 1998
). However, CM cannot be viewed as a polymer with only two states, hydrated and dry. Fruits grow in a wide range of relative humidity and, presumably, the mechanical properties of the CM change according to, though not necessarily in direct proportion to, relative humidity. Fruits also grow in a wide range of temperatures. Peet (1992)
demonstrated a relationship between temperature and the occurrence of fruit cracking, but did not study the mechanical properties of the CM.
In the present work, we describe how the mechanical properties of tomato CM change with relative humidity and temperature, and we introduce relevant new information on the interaction of relative humidity and temperature on the mechanical properties of tomato CM. Ripe tomato fruit CM was employed as a model because the CM of tomato has probably been studied the most extensively. During the last two decades, information on its composition, ultrastructure, and biophysical properties has accumulated (Heredia, 2003
). Data described herein concerning the mechanical properties increase substantially our knowledge about the cuticular membrane at temperatures and relative humidities in the natural environments of crops.
MATERIALS AND METHODS
Culture and sampling
Tomato cv. Cascade was grown in a commercial polyethylene greenhouse in Málaga, Spain (36°40' N, 4°29' W) from mid-February to mid-June 2001, without supplemental heating or lighting. Seeds were sown in vermiculite on 12 January and, when seedlings had developed five true leaves (14 February), 40 plants were transplanted one each into 40 pots of 20-L capacity filled with sand (3 mm diameter). Pots were arranged in rows with 1 m between rows and 2 pots/m within rows. Standard nutrient solution (10 mM N, 7 mM K, 0.9 mM P, 5 mM Ca, 2 mM Mg, and microelements) was supplied to the plants from transplanting to maturity by an automatic trickle irrigation system, with one trickler per plant that dispensed 2.0 L/h. Plants were grown as single stems by removing side shoots at weekly intervals. Flowers were vibrated daily to facilitate pollination. Flowers were labeled at the time of blooming and monitored subsequently to evaluate fruit development and ripening. Fifty fruits were selected when fully ripe for CM isolation and further quality studies. CM were isolated from each fruit within five hours from fruit harvesting.
Cuticle isolation
Fruit CM was enzymatically isolated from ripe tomato fruits following the protocol of Orgell (1955) as modified by Yamada et al. (1964; see Petracek and Bukovac, 1995
) using an aqueous solution of a mixture of fungal cellulase (0.2% w/v, Sigma, St. Louis, Missouri, USA) and pectinase (2.0% w/v, Sigma), and 1 mM NaN3 to prevent microbial growth, all in sodium citrate buffer (50 mM, pH 4.0). Suspensions were aspirated to facilitate enzyme penetration, then they were incubated with continuous agitation at 30°C for 7 to 10 d. The CM was then separated from the epidermis, rinsed in distilled water, and stored in dry conditions.
Mechanical tests
The mechanical properties were measured using an extensometer equipped with a linear displacement transducer (Mitutoyo, Kawasaki, Japan) specifically made to work with CM (resolution of ± 1 µm). The equipment is very similar to that designed and reported by Kutschera and Schopfer (1986)
. Rectangular uniform segments (3 mm x 9 mm) of isolated CM were removed using a metal block and inspected microscopically to check for absence of small cracks, before mechanical testing. The dry CM segments were fixed between the ends of two hollow stainless-steel needles, by a small amount of fast-drying super-glue, such that the CM formed a plane surface (Fig. 1). A container was attached to the extensometer so the samples could be equilibrated in a buffer solution of 20 mM sodium citrate (pH 3.2) with 1 mM NaN3 in order to inhibit bacterial and fungal growth (Kutschera and Schopfer, 1986
; Petracek and Bukovac, 1995
). The system was enclosed in an environment controlled chamber that allowed control of temperature and relative humidity (RH). Every CM sample was maintained inside the extensometer chamber at least 30 min to equilibrate their temperature and humidity with the medium before beginning the extension test.
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The mechanical tests were performed as a transient creep test to determine the changes in length of a CM segment by maintaining samples in uniaxial tension, under a constant load, for 1200 s, during which the longitudinal extension of each sample was recorded by a computer system every 3 s. Each sample was tested repeatedly using an ascending sequence of sustained tensile forces (from 0.098 N to breaking-point by 0.098 N load increments) without recovery time (Fig. 2). To determine stresses, the tensile force exerted along the sample was divided by the representative cross-sectional area of the sample. To obtain the corresponding stress–strain curve, the applied stress was plotted against the total change in length after 20 min. Breaking stress (max) and maximum strain (max) were also determined for each sample.
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Statistics
Simple and multiple regression analyses and all pairwise comparisons of the E, max, and max means were used to determine whether the measured characteristics of the CM samples varied significantly and predictably as a function of humidity and/or temperature. All analyses were performed using the software package JMP (SAS Institute, Inc.) on a Power Macintosh 8100/80. Data are presented as means and SD with a level of significance of 5% (P = 0.05).
RESULTS
Mechanical behavior of isolated tomato fruit CM
The time-course of creep of isolated tomato fruit CM showed two clear phases when loaded in tension by load increases of 0.098 N at intervals of 1200 s at 23°C and 40% RH (Fig. 2). (1) There was a first phase that lasted from 0 to 0.49 N of load (five load increases) in which CM responded to each load by instantaneous extension (about 0.5% strain in every load) but with no further extension recorded until the next load was added; the strain in this phase was purely elastic. (2) There was a second phase, at loads greater than 0.49 N, in which CM responded by instantaneous extension (elastic strain) and by some additional extension (viscoelastic strain) during the time that the same load was maintained. The transition from elastic to viscoelastic was gradual, with elastic strain predominating over viscoelastic strain from 0.49 to 0.784 N (five– eight loads) and viscoelastic being predominant at loads greater than 0.784 N.
Biphasic behavior can also be observed in the stress–strain curve at 23°C and 40% RH where the relationship can be defined by two phases with different slopes (Fig. 3). The stress–strain curves allow the calculation of tensile modulus, E, from the slope of the linear elastic phase of the curve, Ee, and from the linear viscoelastic phase, Ev. The average thickness of the cuticle between the epidermal cell wall and the outer surface was 7.2 ± 0.3 µm. This value was used to estimate the cross-sectional area of the samples. See Fig. 3 for details.
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When CMs were submerged in aqueous solution (wet), the stress–strain curves were monophasic corresponding to viscoelastic strain, and tensile modulus (Evwet = 172 ± 83 MPa) was even smaller than Ee at 80% RH (Fig. 3). Tensile modulus at wet experimental conditions was similar to that obtained from the slope of the second linear phase at 40 and 80 % RH (Ev40% = 201 ± 25 MPa; Ev80% = 182 ± 34 MPa). Tensile modulus in the viscoelastic phase of the stress–strain curve seems to be independent of RH and of temperature (data not shown).
The combined effects of temperature and RH are shown in Fig. 4. Tensile modulus decreased when temperature increased from 10 to 45°C at 40% RH. This decrease was nonlinear but can be described as two temperature-independent stages, at 10–30°C (Ee values about 705 MPa) and at 35–45°C (Ee values about 435 MPa), and with a transition between them at a temperature of 30–35°C. At 80% RH, Ee was smaller that at 40% RH at all temperatures, and although there was still a significant difference between the value of Ee at the lower and higher range of temperatures, the transition between stages was more gradual, extending between 23 and 35°C. At wet conditions, Ev did not differ significantly (P = 0.05) over the range of temperature; however, there were still significant differences at P = 0.07 between the mean Ev at 10 and 23°C and the mean Ev at 35 and 45°C.
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Considering that E was independent of temperature below or upon transition temperature (values of E without significant differences, Table 1), mean values of E were calculated below or above the transition temperature, for 40, 80, and wet. Tensile modulus decreased with increasing RH for temperatures both below and above the transition temperature. In absolute terms, the decrease of E was greater below transition temperature (707–163 MPa) than above (437–99 MPa); however, in relative terms the decrease was similar, 77% in both cases.
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max) could also be described as two stages, below 30 and above 35°C, again with a transition temperature between 30 and 35°C (Fig. 5). Differences of max between high and low temperatures were significant at wet and 80% RH. The low-temperature plateau at 40% RH was unclear because of the large value of max observed at 10°C. Stress at breaking point below and above the transition temperature decreased with increasing RH, although, in this case, the decrease was similar below (32–21 MPa) than above (26–14 MPa) the transition temperature (Table 1).
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Relative humidity and temperature together explained 63% of the variance observed for max (R2 = 0.630, P < 0.001). Similarly to the case of E, RH explained more of the variability in max (R2 = 0.383) than did temperature (R2 = 0.247), although RH and temperature made a similar contribution to the variance of max (38% and 25%, respectively) than of E. Thus, the strength of the CM was affected by both RH and temperature.
Stiffness and strength are related through RH and temperature
The set of 77 CM samples for which both stiffness and strength were measured were used to investigate the relationship between these two parameters. In general, E and max varied in the same direction: the higher or the lower E, the higher or the lower max (Fig. 6). The relation between the two variables could be described by a linear regression (R2 = 0.55, P > 0.99), and no better fit could be achieved using polynomial, logarithmic, exponential equations.
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max were affected by both RH and temperature, we have investigated the relationship between stiffness and strength using sets of CM samples at the same RH and at the same temperature. At RH of 40% or 80%, the change in max produced by changes in temperature between 10 to 45°C only explained 28% of the variance in E; E would increase at a rate of about 7 MPa per MPa increase of max. At wet conditions, E and max were independent (Table 2). At constant temperature of 10, 23, 35, and 45°C, the change in max produced by changes in RH between 40 and wet, explained almost half (44–49%) of the variance in E; E would increase at a rate of about 15 MPa per MPa increase of max. At 30°C, changes in max produced by changes in RH explained a much higher (up to 70%) proportion of the variance in E than at 10, 23, 35, or 45°C. This could be because 30°C was close or in the transition temperature where large changes in E and max were recorded with small changes in temperature.
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max) of CM samples was 13.8 ± 0.5%. No significant differences for max due to temperature or RH were detected. Maximum elongation and stiffness were independent when all (77) data set was considered or when the subsets of the data with the same RH or same temperature were considered. Maximum elongation and maximum strength appeared as independent variables when the whole (77) data set was considered; however, when data were divided according to the same RH, a significant positive relationship was found at 40 and 80% RH (Table 2). This relation between max and max was not found at constant temperature. DISCUSSION
The stress–strain curves of tomato fruit CM revealed a biphasic behavior when tested at RH below 100%. At loads smaller than 0.49 N, the CM was instantly deformed characteristic of elastic behavior. In contrast, at loads greater than 0.59 N, deformation demonstrated a creep process. This biphasic behavior has not been described in previous research on the biomechanics of CM from tomato fruit (Petracek and Bukovac, 1995
; Wiedemann and Neinhuis, 1998
), nor from other fruits. Nevertheless, the biphasic behavior has been reported in other plant tissues as fibers from Agave americana or Cocos nucifera, wood from Juniperus virginiana, strengthening tissues from Fontinalis antipyretrica and Equisetum hyemale, and from stems of Aristolochia species (Köhler, 2000
and references therein) and from leaf cuticles of Nerium oleander and Hedera helix (Wiedemann and Neihuis, 1998
). Köhler (2000)
indicates that, in the case of cell walls of Aristolochia stems, the cellulose microfibrils are responsible for the elastic behavior, whereas the rest of the cell wall matrix accounts for the plastic mechanical alterations. Plant CM can be also considered as a composite biopolymer mainly formed by an amorphous polyester (cutin) and small amounts of waxes, and hydrolyzable polysaccharides, mainly cellulose. The macromolecular arrangement of these biopolymers may provide the molecular basis to explain both elastic and viscoelastic behavior of the tomato CM. This information has been difficult to obtain until now (Heredia, 2003
), but it will be an important area of research to improve our understanding of mechanical properties of plant CM.
Tensile modulus, a direct measure of the sample stiffness, has been used to characterize plant material (Niklas, 1992
; Hershko, 1994
) and to quantify the responses of a material to variables such as temperature and RH (Murase and Merva, 1977
; Hole, 2000
). Our values of E for isolated tomato fruit CM are not far from those reported by Matas et al. (2004a)
and Wiedemann and Neinhuis (1998)
for a wide number of isolated CM from fruits and leaves.
Data presented in this paper indicates that mechanical properties of the isolated tomato fruit CM depend on relative humidity and temperature, as do other biological polymers as cellulose. Tensile modulus and maximum strength of the CM samples varied in the same direction with RH and temperature: the higher the RH and temperature, the lower both stiffness and strength. The dependence of E on RH and temperature has been demonstrated only in the elastic phase of the strain– stress curve; tensile modulus calculated in the viscoelastic phase, Ev, was independent of both environmental variables, indicating that RH and temperature affected the structural component responsible of stiffness only in the elastic phase of the curve. Additionally, stiffness and strength can be related through RH and temperature.
Although earlier research on the biomechanics of CM isolated from tomato fruit described a reduction on E after hydration or removal of waxes (Petracek and Bukovac, 1995
; Wiedemann and Neinhuis, 1998
), none of these authors reported the effects that relative humidity and temperature could have over the mechanical properties of the fruit CM.
The presence of water in the CM samples is a primary determinant of their mechanical properties. We have found that the stiffness of the CM was reduced after immersion of the CM in water, confirming the results obtained by Petracek and Bukovac (1995)
and Wiedemann and Neinhuis (1998)
. In addition, we have characterized the mechanical properties of submerged CM samples, demonstrating that they presented viscoelastic behavior that followed a linear, monophasic stress– strain curve, showing the smallest tensile modulus and stress at maximum load. Below 100% RH, the stress–strain curve was biphasic, and a negative relationship between E and RH was found. However, to develop a complete and plausible explanation of the effect of RH on the mechanical properties of the CM, temperature must be also considered. Moreover, as our results revealed, the effects of both temperature and RH on stiffness and stress were closely related.
Temperature decreased Ee and stress of isolated tomato fruit CM. This relationship, a typical feature observed also for technical semicrystalline polymer like polyethylene, was not linear but showed two temperature-independent stages separated by a transition temperature between 23 and 35°C, depending on the RH at which measurements were made. These characteristics of the temperature response of E and of stress can be related to the presence of a temperature transition in the cutin matrix of the isolated tomato fruit CM. The existence of a second order (glass) transition temperature in the cutin matrix of isolated tomato CM has been reported recently by members of our laboratory after differential scanning calorimetric analysis of the specific heat of isolated tomato fruit CM and the corresponding isolated cutins (Matas et al., 2004b
). Cutin samples presented a clear second-order transition (named glass transition) temperature in the range of 18–30°C. The transition temperatures of isolated cutin and tomato CM are similar though not identical, perhaps because the CM contains waxes and polysaccharides (mainly cellulose) in addition to cutin. The presence of a transition temperature in the CM and in the cutin matrix of the same samples, suggests the coexistence, over a physiological range of temperature, of two physical states with different structural characteristics. Below the transition temperature, the polyester that forms the cutin would remain with restricted rotational and vibrational freedom in addition to an effective loss of translational motion. Above the transition temperature, the molecular arrangement of the polymer would be more relaxed and dynamic, permitting translational motion between the long hydrocarbon chains present in the cutin network. This could provide a macromolecular explanation for the biomechanical behavior of fruit CM observed and described here: greater stiffness associated with a glass state below the transition temperature and plastic characteristics, being associated with a more viscous state, above the transition temperature.
Water plays a crucial role in this complex scenario. For tomato fruit CM, the phase transition is, from the energetic point of view, attenuated, and that transition shifted to lower temperature, when water is sorbed by CM. This would indicate plasticization of the main component of the CM samples, the cutin matrix (Matas et al., 2004b
). Accordingly, the transition temperature was lowered when humidity increased, and a transition was hardly apparent when isolated CM samples were totally submerged (seen in Fig. 5 for E as function of temperature and RH). In addition, isolated tomato fruit CM can sorb variable amounts of water as a function of the water activity or relative humidity (Luque et al., 1995
). The plasticizing effect in polymer science can be described in terms of lowering the fracture strength, elastic modulus, and viscosity of the biopolymer-water mixtures with an increase in plasticizer content. The plasticizing effect of water may be due to the weakening of hydrogen bonds and other intermolecular interactions within the matrix by the shielding of these (mainly attractive) forces by water molecules. In other words, the results presented here suggest that hydration of CM would be an essential source of CM plasticity. This interpretation agrees well with the description by Round et al. (2000)
of the nanomechanics of isolated cutin of tomato fruits using atomic force microscopy.
In summary, hydration and temperature have important effects on the stiffness and strength of tomato CM. Furthermore, although there is no a priori theoretical relationship between E and max, our results show that stiffness and strength are linearly related. Considering that stiffness and strength in a composite biomaterial, like tomato fruit CM, depend on the biomaterial components (mainly cutin and polysaccharides in tomato fruit CM) and on the structural relation between those components, the empirical correlation observed here between stiffness and strength would indicate the effect of water and temperature on the structural relation of CM components. Further studies are necessary to elucidate which are the structural bases of the mechanical behavior of the CM and how the structural arrangement between those components are modified or changed by the effect of water content and temperature.
Maximum elongation before breaking was constant at the wide range of temperature and RH tested. In this case, the energy absorbed by the material before breaking was proportional to the stress applied to break the sample. Considering the case of a tomato fruit, the relaxation of internal pressure due to CM elongation would be similar in different environmental conditions, so that the breaking of the fruit CM will depend only on the stiffness of the material and on internal pressure.
The results of the research described here can be related to experimental observations of two of the main environmental factors associated with cracking of tomato fruit: the presence of water in the form of rain (high RH) or water condensed on the skin of the fruit, and high fruit temperature, either because of elevated air temperature or because of direct exposure of the fruit to sunlight (Emmons and Scott, 1997
). Thus, data presented in this paper helps us to understand the economically important and complex physiological phenomenon of fruit cracking. From a more biophysical point of view, the elastic and viscoelastic properties of isolated CM remain to be elucidated at the molecular level. Nevertheless, as our work demonstrates, the combined effect of hydration and temperature seems critical in explaining the biomechanics of tomato fruit CM, providing the bases of a possible model to explain fruit CM cracking.
FOOTNOTES
1 This work was partially supported by CAJAMAR in collaboration with CSIC and Universidad de Málaga. Antonio J. Matas was funded by a grant from Ministerio de Educación y Ciencia. The authors thank Drs. Karl J. Niklas and Anthony R. Yeo for helpful discussion and comments. 
4 Author for correspondence (heredia{at}uma.es
) Phone: 34-952-131940, fax: 34-952-132000
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), 80% (
), and 100% RH (
). Temperature was constant at 23°C
), 80% RH (•) and 100% RH (
). Data are means ± SD