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Ecology |
Centro de Investigación Científica de Yucatán, Calle 43 No. 130, Col. Chuburná de Hidalgo, C.P. 97200, Yucatán, México
Received for publication August 7, 2003. Accepted for publication December 4, 2003.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: Crassulacean acid metabolism • dew • drought • photoprotection • threatened species • Tillandsia • vertical distribution • Yucatan, Mexico
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Zotz and Hietz, 2001
). The capacity for photoprotection as well as for shade tolerance has also been correlated with vertical position in the canopy (Benzing, 1990
; Griffiths and Maxwell, 1999
), and different abilities to acclimate to photosynthetic photon flux density (PPFD) may allow epiphytes to coexist at different positions within the same host trees (Werneck and Espírito-Santo, 2001
). Seasonal environmental variations and the deciduousness of host trees can dramatically change light conditions within the canopy (Zotz and Winter, 1994
; Nobel and De la Barrera, 2003
), and the ability to acclimate to changes in light environment may be important for some epiphytic bromeliads (Maxwell et al., 1992
, 1995
).
Because canopies in dry forests tend to be more open than tropical rain forests, gradients in humidity and exposure are not as great and there is little or no vertical stratification of epiphytes (Benzing, 1990
; Zimmerman and Olmsted, 1992
). The presence of the water-conserving Crassulacean acid metabolism (CAM) in epiphytes is correlated with reduced water availability (Benzing, 1990
), and in drier tropical forests the proportion of epiphytic CAM species is high (Zotz and Hietz, 2001
). Observed vertical stratification of CAM epiphytes in the tropical dry forest thus may be the result of differences in photoprotection ability or shade tolerance rather than differences in tolerance to water availability and drought.
This study was performed to investigate the microhabitats and physiological responses of two congeneric epiphytic CAM bromeliads with similar adult sizes, but with different morphologies that occur on the same host trees in a dry deciduous forest in southern Mexico. Tillandsia brachycaulos is an atmospheric-type bromeliad with succulent leaves, and T. elongata var. subimbricata is a tank-forming bromeliad with leaves that are much less succulent. The vertical distribution, and thus the light environments, of the two species have been anecdotally regarded as distinct, with T. brachycaulos occurring lower in the canopy than T. elongata. We hypothesize that different within-tree distributions of these two species is a result of their different capacities for photoprotection or tolerances to shade more than their different tolerances to drought, because of the open nature of the dry forest where they co-occur and because they both exhibit CAM (Griffiths et al., 1986
; Martin, 1994
). Thus, based on canopy position, the less-exposed T. brachycaulos would have less capacity for photoprotection, greater tolerance of shade, and possibly less tolerance of drought than the more-exposed T. elongata.
Field measurements of the light environment were made above individuals of both species co-occurring on the same host trees to avoid complications of host-tree specificity and both field and laboratory measurements of chlorophyll fluorescence were made to quantify their capacity for photoprotection. Greenhouse experiments measuring carbon accumulation in leaves at night coupled with laboratory measurements of instantaneous net CO2 uptake by whole plants were performed to determine the effects of the light environment and water stress on carbon accumulation. Additionally, the effect of light quality on seed germination was tested as an alternative explanation for the observed vertical stratification of adult plants.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). The site receives 650–700 mm annual rainfall with an average mean air temperature of 25.8°C, a maximum of 45°C, and a minimum of 10°C (Thien et al., 1982
). Most of the trees are leafless during the marked dry season that occurs from December to May.
Tillandsia brachycaulos Schlechtendal occurs from southern Mexico to Venezuela (Smith and Downs, 1977
) and is abundant at the study site. Seedlings are common but 60% of the individuals are the result of asexual propagation by sympodial branching (Mondragón et al., 1999
). Tillandsia elongata var. subimbricata (Baker) L. B. Smith is less common at Dzibilchaltún and in Mexico is restricted to the tropical deciduous forest of the northern part of the Yucatán Peninsula (Olmsted and Gómez-Juárez, 1996
). Tillandsia elongata is considered a threatened species in the Protection of Natural Resources Document by the Mexican government (NOM-ECOL-059-1994
) and its range extends to South America (Smith and Downs, 1977
). Vegetative propagation for T. elongata is rare at the study site (F. Chi, Centro de Investigación Científica de Yucatán, personal communication). Tillandsia brachycaulos is considered atmospheric (ecophysiological type V, according to Benzing, 2000
), although it has some water impoundment capacity, and T. elongata produces a well-developed tank (type IV; Benzing, 2000
). Both species have wind- dispersed seeds of similar size.
Field measurements
The location of all individuals of each species was recorded in the canopies of 11 host trees that were selected because they supported at least five individuals of the less common T. elongata. Six of the host trees are deciduous species. Height above the ground for each individual was measured with a flexible tape measure and tree height was calculated geometrically with distance and angle measurements. Photosynthetic photon flux density was measured for approximately 48 h about 20 mm above each T. elongata occurring in each host tree (mean number of individuals per tree ± SE = 7.4 ± 1.2) and above randomly selected T. brachycaulos (8.8 ± 0.6 individuals/tree) using gallium arsenide phosphide photodiodes (Pontailler, 1990
; Hamamatsu, Bridgewater, New Jersy, USA). Diodes were calibrated against a quantum sensor (LI-COR, Lincoln, Nebraska, USA) and measurements were collected every 5 s using a solid-state data logger (CR21X and CR10X, Campbell Scientific, Logan, Utah, USA) in reference to two additional sensors placed above the canopy at approximately 15 m above the ground. Dry season PPFD measurements were made from 11 to 29 May 2001 for 131 individuals of T. brachycaulos and 72 of T. elongata. Wet season measurements were made from 19 September to 10 October 2001 above the same individuals; however, only 110 T. brachycaulos and 62 T. elongata persisted because wind had caused the others to fall from their locations.
Maximum quantum efficiency was measured as dark-adapted chlorophyll fluorescence (Fv/Fm) in the field with a portable fluorometer (Plant Efficiency Analyzer, Hansatech Instruments, Kings Lynn, UK) during the rainy season from 3 to 9 October 2001. Measurements were made on 45 randomly selected individuals of each species at dawn on one mid-rosette leaf per individual; leaves were maintained dark-adapted by being covered with opaque clips placed the previous late afternoon.
Laboratory measurements
Plants were collected in the field and maintained with at least weekly watering under neutral-density shade cloth providing approximately 55% ambient PPFD. Individuals of T. brachycaulos used for laboratory measurements averaged 16.4 ± 1.9 g (n = 12) hydrated fresh mass without tank water and 94 ± 6 mm in diameter, and T. elongata averaged 14.0 ± 2.8 g and 99 ± 8 mm in diameter.
Fresh mass without tank water was obtained for cleaned plants with dead leaves removed that had been watered daily for at least 1 wk. These plants were submerged in water for 3 h and then inverted and air dried for 4 h in the laboratory to remove surface and tank water before their mass was measured. Mass with tank water was obtained by submerging plants and then allowing upright, filled plants to drain excess water for 1 h in the laboratory. For the drought experiment, plants were placed outside the laboratory on 15 November 2001 under translucent plastic with a PPFD transmission of approximately 40% and which intercepted rain and prevented dew formation on the plants.
Fluorescence of well-watered collected plants was measured after dark- adapting their leaves for at least 12 h, similar to field plants, and using the same portable fluorometer that was used in the field. To determine the potential for thermal dissipation of energy, non-photochemical quenching (NPQ) was estimated using dark relaxation kinetics, a technique that allows the use of a non-modulated fluorometer (Walters and Horton, 1991
; Maxwell and Johnson, 2000
). Even though deconvoluting NPQ solely by analysis of dark relaxation kinetics is not robust (Walters and Horton, 1991
), such analysis can be useful for qualitative comparisons for plants under identical conditions. Two mid-rosette leaves per plant were exposed to a PPFD of 1000 µmol · m–2 · s–1 for 1 h, supplied by a halogen lamp, and then placed in darkness followed by fluorescence measurements at 0.5, 5, 10, and 45 min. Values of light-adapted Fm were calculated by logarithmic extrapolation of recovering Fm and NPQ was resolved into two components (Walters and Horton, 1991; Maxwell and Johnson, 2000
): rapidly relaxing (NPQfast) and slowly relaxing (NPQslow, using the value of Fm obtained at 45 min of darkness).
Pigments were extracted from leaves collected from mid-rosette for plants maintained for at least 4 wk under neutral-density shade cloth for either high light (74.2% total daily PPFD) or low light (6.5% PPFD) treatments. Approximately 900 mm2 of leaf tissue was collected in the morning and immediately frozen in liquid nitrogen; the tissue was later macerated in 20 mL ice-cold 80% acetone made alkaline with 0.1 g NaHCO3. Concentrations of chlorophyll a, b, and total carotenoids were measured with a spectrophotometer (DU-65, Beckman Coulter, Fullerton, California, USA) according to equations published by Wellburn (1994)
.
Titratable acidity was measured for plants collected in the field from exposed, intermediate, and shaded locations that had been acclimated to the appropriate shade treatments for 5 wk; plants were watered approximately every other day during the week before measurements. Three to four leaves per plant were collected at dusk between 1900 and 2020 on 10 June 2002 and between 0530 and 0630 the following day; total daily unshaded PPFD was 57.37 mol/m2. Leaf acidity was quantified from frozen leaf tissue by boiling chopped leaves in distilled water for 5 min and titrating the resulting solution with 0.01 mol/L NaOH to a pH of 7.0 (Pearcy et al., 1989
) as measured with an electronic pH meter (Model 744; Metrohm, Herisau, Switzerland).
Gas exchange was measured for whole plants in 1.86 x 10–3 m3 cylindrical aluminum chambers sealed with a glass window at one end through which 1000 µmol · m–2 · s–1 PPFD for 12 h/d was provided with a 50-W halogen lamp filtered through 120 mm distilled water to reduce heat load. Temperatures were maintained at approximately 30°C during the day and 25°C at night by convective cooling of the chambers. Relative humidity within the chambers was that of the ambient air, approximately 40% during the day. Four such chambers were connected with a set of solenoid valves to an infrared gas analyzer (LI-6400; LI-COR) such that gas exchange data was collected automatically every 40 min for each plant for 24 h. Temperatures were maintained at approximately 30°C.
Drought was defined as commencing with the withholding of daily watering. During the drought experiment, senesced dead leaves and leaf tips were periodically removed, dried, and weighed; hydrated fresh mass used in calculating percentage water loss was thus adjusted for the loss of living tissue. Thermocouple sample chambers (C-52; Wescor, Logan, Utah, USA) and a microvoltmeter (HR-33T; Wescor) were used to measure the water potential of approximately 3–5 disks 6 mm in diameter (approximately 0.06 g fresh mass) of leaf tissue collected mid-leaf and mid-rosette for six individuals of each species before and after drought.
Specific leaf mass was calculated from the projected area and dry mass of whole leaves dried at 60°C for 48 h. Projected area was determined using digital photographs of whole leaves gently flattened under a thin piece of low- reflectance glass and a freeware computer program (Scion Image, Scion, Frederick, Maryland, USA) that calculated area from the photographs. Leaf succulence was calculated as the difference between hydrated fresh mass, determined after placing leaves in a sealed container in contact with paper towels saturated with distilled water at 4°C for 48 h, and dry mass and is expressed on a projected area basis.
To determine the light requirements for seed germination, closed seed capsules were collected in the field and seeds were removed under a green safe- light providing 0.007 W/m2. Approximately 30 seeds from each species were placed into different halves of 12 transparent Petri dishes lined with moist filter paper. A random one-third of the Petri dishes were wrapped in two layers of aluminum foil as a dark control. The remaining dishes were exposed to six 1-h periods per day of 0.5 W/m2 of either red light, provided by a 15-W compact fluorescent lamp wrapped in red cellophane, or far-red light, provided by a 10-W incandescent lamp wrapped in blue and red cellophane and filtered through 11 cm of distilled water. Irradiance was measured with an electronic pyranometer (LI-200SA; LI-COR). All Petri dishes were maintained in a temperature-controlled chamber at 27°C for 7 d before scoring for germination.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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During the dry season after the host trees had dropped most of their leaves, the average daily PPFD received by T. brachycaulos was 41.8 ± 1.2% of ambient and that by T. elongata was 58.2 ± 1.4% (Fig. 1A; P = 0.0001; t = 8.28). During the wet season when host trees were fully leafed, the average daily PPFD received by T. brachycaulos was 10.8 ± 1.2% and that by T. elongata of 26.5 ± 2.3% (Fig. 1B; P = 0.0001; t = –6.66). Tillandsia brachycaulos received an average of 8.7 ± 0.9 times more PPFD during the dry season compared to the wet season and T. elongata received 2.6 ± 0.6 times more. Average daily PPFD above the canopy for the dates during the dry season was 45.4 ± 2.6 mol · m–2 · d–1 and for the wet season was 39.3 ± 3.3 mol · m–2 · d–1 (P = 0.1). The vertical distribution of each species within host trees was superficially similar to the distribution of PPFD received by each species during the dry season (Fig. 1A), although the correlation between height and exposure to PPFD for individuals of each species was weak (r2 = 0.15).
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Nonphotochemical quenching and maximum quantum efficiency
Fast-relaxing nonphotochemical quenching (NPQfast) was lowest for T. brachycaulos acclimated to high PPFD conditions (Table 1). Each species had more NPQfast capacity in individuals acclimated to low PPFD compared to high PPFD. The NPQslow was also greater in individuals acclimated to lower light conditions compared to high light (Table 1; species combined P = 0.021; t = 2.59).
Maximum quantum efficiency (Fv/Fm) during the rainy season for both species in the field decreased equally with exposure (Fig. 2). The Fv/Fm was highest for individuals in shaded locations receiving less than about 20% daily PPFD (0.81 ± 0.01; n = 20 each species, data combined). For the 10 individuals of each species in the most exposed locations, average daily PPFD was about 62% of that at the top of the canopy and Fv/Fm averaged 0.72 ± 0.01 (data combined).
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Drought and responses to rewatering
The external water reservoir (tank water) volume of T. brachycaulos 1 h after irrigation was about 54% of that of T. elongata, relative to total hydrated mass. Within the first day of drought, T. brachycaulos had lost all tank water, whereas T. elongata required a little more than 2 d to lose its tank water under similar conditions (Fig. 5A). After 30 d of drought, T. brachycaulos had lost about 44% of its hydrated mass and T. elongata had lost 32%. After 30 d of drought, T. brachycaulos also had senesced leaf tissue, averaging 2.3 ± 0.7% of its hydrated mass and consisting mostly of leaf tips; senescent tissue of T. elongata was 21.7 ± 2.7% of its hydrated mass and included entire older leaves and large distal portions of younger leaves. Water potential of leaf tissue before drought was similar for the two species and averaged –0.44 ± 0.07 MPa (n = 6 each species). Water potential at 30 d of drought also did not differ between species and averaged –0.89 ± 0.08 MPa (P < 0.005; t = –3.57).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Maxwell et al., 1992
; Griffiths and Maxwell, 1999
). The chlorophyll a : b ratio increased significantly with decreased PPFD for T. elongata and nonsignificantly for T. brachycaulos, opposite to the pattern for most plants but previously noted for other epiphytes (Gauslaa and Solhaug, 1996
), and may indicate a reduction in the number of photosynthetic reaction centers (Osborne et al., 1994
).
Because T. elongata occurred in more exposed locations, we expected it to have a greater capacity to dissipate excess light energy as non-photochemical quenching (NPQ; Johnson et al., 1993
) than did T. brachycaulos. However, the maximum quantum efficiency (dark-adapted Fv/Fm) decreased similarly for both species during the wet season in the field in increasingly exposed locations, suggesting that both species experience similar long-term, photo-oxidative damage under similar high PPFD conditions; it is predicted that photo-oxidative damage during the dry season for both species in all exposures would be even greater. Individuals of both species had similar levels of NPQslow or irreversible photo-oxidative damage (Walters and Horton, 1991
) after being exposed to relatively high light in the laboratory; however, they had less NPQslow than some shade-tolerant epiphytic bromeliads (Griffiths and Maxwell, 1999
). Individuals of both species also had similar NPQfast, implying similar capacity for the light-induced formation of photoprotective zeaxanthin (Walters and Horton, 1991
; Demmig-Adams and Adams, 1992
). Values of NPQfast were similar to those previously recorded for T. elongata, and the species previously has been characterized as a high-light- adapted species (Griffiths and Maxwell, 1999
). Tillandsia brachycaulos had the lowest potential for NPQfast when it occurred in exposed locations, however, suggesting that it may be less able to acclimate to high light than can T. elongata.
When well-watered, T. brachycaulos can fix up to 12% of its total net carbon uptake during the daytime, presumably using the C3 or mixed C3-CAM photosynthetic pathways. Tillandsia elongata can fix up to 23% during the daytime, indicating a similar photosynthetic flexibility in response to water availability. Most atmospheric-type bromeliads like T. brachycaulos are reported to be obligate CAM plants, although this observation is often based on integrative measurements such as stable isotope 
13C values (Smith et al., 1986a
; Zotz, 2002
) or nocturnal acidity (Smith et al., 1986b
), which may not fully demonstrate photosynthetic flexibility (Pierce et al., 2002
; Winter and Holtum, 2002
). One hundred percent of the carbon gain for well-watered T. elongata occurs at night for individuals collected from a Panamanian seasonally dry rain forest (Pierce et al., 2002
), in contrast to the data presented here for the same species under similar conditons. This suggests that the flexibility of CAM (Pierce et al., 2002
; Zotz, 2002
) may differ within a species, possibly confounding recent attempts to classify species in terms of capacity for CAM (Sayed, 2001
).
The greatest nocturnal acid accumulated for well-watered T. brachycaulos was under a low PPFD (about 30%), and increased PPFD reduced the acid accumulated, suggesting that T. brachycaulos is a shade-adapted species. Nocturnal acid accumulation saturated at low PPFD for T. elongata as well, but decreased only at the highest PPFD, suggesting that T. elongata is able to acclimate to a wider range of light environments. The reduced carbon uptake under high PPFD of adult individuals of T. brachycaulos may exclude it from highly exposed areas.
Leaf water potentials were similar for both species after prolonged drought and similar to those of other bromeliads (Benzing, 1990
; Stiles and Martin, 1996
; Zotz and Andrade, 1998
). Tillandsia brachycaulos lost a larger percentage of water from its succulent leaves compared to the less succulent T. elongata. Even though the leaf tissues of T. elongata have a higher desiccation tolerance than T. brachycaulos (Andrade, 2003
), a large proportion of older leaves and large distal sections of younger leaves of T. elongata died as drought progressed, amounting to approximately 22% of its total hydrated mass before drought. Tillandsia brachycaulos lost much less biomass during drought. The large loss of leaf area for T. elongata during drought indicates that is has a much lower tolerance to drought than does T. brachycaulos. The sacrifice of leaf tissue in T. elongata may have helped maintain high water potentials in living leaves and may be similar to the within-plant transfers of water reported for Mesembryanthemum crystallinum under drought stress (Adams et al., 1998
).
Germination response to quality of light did not differ between species and was completely inhibited by far-red radiation, similar to the case for other epiphytic bromeliad species (Downs, 1964
) and suggesting present within-tree distribution patterns were thus probably not the result of different light- related germination between species. Differences in water relations in the seedling stage may explain the distribution of adults when a more exposed species has seedlings that have a lower transpiration rate than a less exposed species (Zotz and Andrade, 1998
). However, seedling mortality in the field for both species is similar, up to 71% for T. brachycaulos (Mondragon et al., 1999
) and up to 65% for T. elongata (F. Chi, Centro de Investigación Científica de Yucatán, personal communication) and is presumably due to desiccation during the dry season (Mondragon et al., 1999
). The seedlings of both T. brachycaulos and T. elongata species lack appreciable water impoundment capacity, are difficult to distinguish from each other, and their net CO2 uptake rates are similar. Indeed, many bromeliads have drought-tolerant seedlings and slowly shift to a drought-avoiding and tank-forming adult form (Schmidt and Zotz, 2001
), as does T. elongata, and to a much lesser extent does T. brachycaulos. However, further investigation on the occurrence of differential seedling survival is necessary to examine the role of this life stage in determining the observed vertical distribution pattern.
Contrary to our hypothesis, large differences in photoprotection ability did not appear to fully explain the segregation of these two bromeliads along a light gradient. Additionally, T. elongata, which occurs in more exposed locations in the canopy than does T. brachycaulos, is much less drought tolerant than T. brachycaulos, contrary to expectations. Indeed, Tillandsia brachycaulos withstood almost 1 mo of drought before total daily net CO2 uptake became negative, similar to other atmospheric-type bromeliads (Stiles and Martin, 1996
), whereas similar-size individuals of T. elongata withstood a drought of less than 10 d and lost a relatively large amount of leaf biomass after 30 d drought. The exposed locations where T. elongata tend to occur, however, may receive more tank- filling rainfall; lower in the canopy where fewer T. elongata occur, rainfall may be intercepted by overhead tree branches and leaves (Voth, 1939
; Andrade and Nobel, 1997
), possibly favoring the persistence of more drought-tolerant species like T. brachycaulos.
Drought in this region of Mexico is regular and prolonged, sometimes extending to 30 d. Dew formation even during the dry season, however, can be a frequent event (Andrade, 2003
) and may be an important source of water for some bromeliads (Smith et al., 1986b
). Indeed, for the drought experiment, individuals were protected from rainfall as a precaution but were protected from daily dew formation as a necessity. Individuals higher in the canopy receive more dew than those in less- exposed locations (Nobel, 1999
; Andrade, 2003
), reducing their dependence on rain events. The amount of dew would not usually be sufficient to fill the tank of a bromeliad (Andrade, 2003
), however it may be enough to reduce drought stress experienced by leaves covered with water-absorbing trichomes. Thus, the lower drought tolerance of the bromeliad located higher in the canopy suggests that greater exposure may be correlated with greater or more frequent water availability.
The largest difference measured between these two species is the relatively low drought tolerance of T. elongata compared to T. brachycaulos rather than a difference in capacity for photoprotection. Indeed, T. elongata occurs more commonly in wetter forests and may be at the edge of its distribution in terms of its drought-tolerance. Exposed positions in the canopy that allow for more access to precipitation and dew formation may thus allow T. elongata to persist in this tropical dry forest.
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FOOTNOTES |
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LITERATURE CITED |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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