Western North American Naturalist

Volume 60 Number 2 Article 8

5-24-2000

Effect of salinity and planting density on physiological responses of Allenrolfea occidentalis

Bilquees Gul University of Karachi, Pakistan

Darrell J. Weber Brigham Young University

M. Ajmal Khan University of Karachi, Pakistan

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Recommended Citation Gul, Bilquees; Weber, Darrell J.; and Khan, M. Ajmal (2000) "Effect of salinity and planting density on physiological responses of Allenrolfea occidentalis," Western North American Naturalist: Vol. 60 : No. 2 , Article 8. Available at: https://scholarsarchive.byu.edu/wnan/vol60/iss2/8

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EFFECT OF SALINITY AND PLANTING DENSITY ON PHYSIOLOGICAL RESPONSES OF ALLENROLFEA OCCIDENTALIS

Bilquees Gul1, Darrell J. Weber2, and M. Ajmal Khan1

ABSTRACT.—Physiological responses of Allenrolfea occidentalis to salinity and seedling density were investigated. Effects of salinity (0, 200, 400, 600, 800, and 1000 mM NaCl) and 3 planting densities (2000, 4000, 6000 plants m–2) on the growth, survival, and ecophysiology of A. occidentalis, a stem succulent inland halophyte, were studied under con- trolled greenhouse conditions. Plants were grown in a sand culture using subirrigation. Dry mass of roots was highest at 600 mM NaCl at low density (2000 plants m–2), but declined as salinity increased. Tissue water content was highest at the 200 mM NaCl treatment and decreased with increased salinity. Water potential of the plants became more negative with increasing salinity due to the accumulation of NaCl in the leaves. Inorganic ions, especially Na+ and Cl–, con- tributed substantially to dry mass. Na+ and Cl– concentration in shoots and roots increased when NaCl level was + ++ ++ –– – increased while K , Ca , Mg , SO4 , and NO3 contents decreased. Net photosynthesis increased at low salinity (200 mM), but photosynthesis at other salinities was not significantly different from the control. While A. occidentalis is very salt tolerant and photosynthesis functioned reasonably well at high salinities, extremely high salinity did decrease dry mass of roots and shoots.

Key words: salinity, planting density, Allenrolfea occidentalis, halophyte, salt tolerance, pickleweed.

Halophytes are plants that complete their usually do not recruit through seeds, and ram- life cycle at high salinities (Flowers et al. 1977), ets are competitively superior to genets at the and their survival in salt marshes depends on recruitment phase of the life cycle (Gul and salt tolerance at different stages of their life Khan 1999). In a saline habitat dominated by cycle (Adam 1990). Dry mass of halophytes perennials, drought, temperature, and salinity usually decreases with increases in salinity stress synergistically cause death of seedlings (Ungar 1991), although growth of several halo- and depress growth of adult plants. Mortality phytes is stimulated at some levels of salinity in perennial halophytes occurs at the seedling (Flowers and Yeo 1986, Munns et al. 1983, stage due to high salinity, temperature, or Khan and Aziz 1998). Nevertheless, high NaCl severe drought, while adult plants enter into a concentration is probably not essential for phase of dormancy to avoid death (Khan and optimal growth of most halophytes. There are Aziz 1998). several halophytes that show optimal growth Osmotic active adjustment under saline con- at NaCl concentrations of 400 mM or higher, ditions may be achieved by ion uptake, syn- e.g., Cress critic (425 mM NaCl; Khan and thesis of osmotica, or both (Cheesman 1988, Aziz 1998), Suaeda fruticosa (400 mM NaCl), Popp 1995). Halophytes differ widely in the Haloxylon recurvum (400 mM NaCl), and sev- extent to which they accumulate ions and eral cold-desert halophytic species like Sal- overall degree of salt tolerance (Glenn et al. icornia rubra, S. utahensis, Suaeda moquinii, 1996). Stem- and leaf-succulent chenopods are and Kochia scoparia (600 mM NaCl; Khan et commonly known as salt accumulators and al. unpublished data). have high Na+ and Cl– content (Breckle 1975, Intraspecific competition may influence Albert and Popp 1977, Gorham et al. 1980, survival, growth, and fecundity of annual pop- Neumann 1997, Khan and Aziz 1998). Halo- ulations in saline habitats (Ungar 1991). How- phytes have adapted to highly saline condi- ever, the role of competition in perennial pop- tions by their ability to adjust osmotically to ulations appears to be limiting in reference to increasing salinity levels (Reihl and Ungar new recruitment (Khan and Aziz 1998, Gul 1982, Clipson et al. 1985). Tolerance of photo- and Khan 1999). Most perennial halophytes synthetic systems to salinity is associated with

1Department of Botany, University of Karachi, Karachi-75270, Pakistan. 2Department of Botany and Range Science, Brigham Young University, Provo, UT 84602. Corresponding author.

188 2000] PHYSIOLOGICAL RESPONSES OF ALLENROLFEA OCCIDENTALIS 189 the capacity of plant species to effectively after planting. Seedlings were thinned by compartmentalize ions in the vacuole, cyto- removing excess plants from the pots to pro- plasm, and chloroplast (Reddy et al. 1997). duce 3 treatment densities equal to 2000, Chlorophyll fluorescence, an analytical tool for 4000, and 6000 plants m–2. Plants were grown investigating stress damage mechanisms, has for 1 wk in a greenhouse by subirrigation by been used for detecting tolerance to chilling, placing the pots in plastic trays containing freezing, drought, and air pollution stress. It half-strength Hoagland’s solution; the 2nd wk may prove equally useful for salinity tolerance different salinities were applied. Plants were screening (Mekkaoui et al. 1989, Monnieveux subirrigated by placing the pots in plastic et al. 1990) or for detecting salt effects before trays and adjusting the water level daily to visible damage occurs (West 1986). correct for evaporation. Once weekly we com- Allenrolfea occidentalis (Wats.) Kuntze pletely replaced salt solutions to avoid buildup (Chenopodiaceae), a C3 plant common in the of salinity in pots. At the initiation of the western U.S., is found in an environment experiment, we gradually increased salinity where halomorphic soil induces extreme concentrations by 200 mM at 1-d intervals osmotic stress in concert with erratic and low until the maximum salinity level of 1000 mM precipitation during the growing season (Trent NaCl was obtained. Seedlings were grown in a et al. 1997). During drought this species ex- greenhouse at a thermoperiod of 25°C:35°C hibits low photosynthesis, stomatal conductance, (night:day) for a total of 90 d after final salinity and transpiration in comparison to years with concentrations were reached. high moisture (Skougard and Brotherson 1979). Dry mass of plant shoots and roots was Allenrolfea occidentalis is restricted to a few measured 90 d after the highest salt concen- communities directly at the margin of playas tration was reached. Dry mass of plants from where soils are often poorly drained and have an individual pot was determined after drying high soil salinity (Hansen and Weber 1975). for 48 h in a forced-draft oven at 80°C. Ion Because little information is available on concentration was determined by boiling 0.5 g the growth and salt tolerance of Allenrolfea of plant material in 25 mL of water for 2 h at occidentalis, the objective of this study was to 100°C using a dry-heat bath. This hot water determine the physiological responses of A. extract was cooled and filtered using Whatman occidentalis to salinity and seedling density. no. 2 filter paper. One mL of hot water extract We hypothesized that increased salinity and was diluted with distilled water for ion analy- seedling density would decrease the growth sis. Chloride, nitrate, and sulfate ion contents response of A. occidentalis. were measured with a DX-100 ion chromato- graph. Cation contents, Na+, K+, Ca2+, and MATERIALS AND METHODS Mg2+, of plant organs were analyzed using a Perkin Elmer model 360 atomic absorption We collected Allenrolfea occidentalis seed- spectrophotometer. lings from an inland salt playa located on the Using an LI-6200 portable photosynthesis east of Goshen, in northwestern Utah (39:57: system (LI-COR, Inc., Lincoln, NE), we mea- 06N 111:54:03W, 4530 ft). Equal-sized seed- sured the net CO2 assimilation rate of 4 plants lings (about 1 sq cm in size) were transplanted for each treatment. Level of stress in plants into 12.7-cm-diameter × 12.7-cm-tall plastic growing at different salinities was determined pots containing nutrient-free sand. We used 3 to be the amount of fluorescence measured planting densities (low, 25 plants per pot, from photosystem II with a Morgan CF-1000 which was equal to the rate of 2000 plants chlorophyll fluorescence measurement system m–2; medium, 50 plants per pot, equal to the (P.K. Morgan Instruments, Andover, MA). Stress –2 rate of 4000 plants m ; and high, 75 plants is measured as a ratio of Fv (variable fluores- –2 per pot, equal to the rate of 6000 plants m ). cence) to Fm (maximum fluorescence). Water Six salinity (0, 200, 400, 600, 800, and 1000 potential was measured at midday with a pres- mM NaCl) treatments were used. Four repli- sure chamber (PMS Instrument Co., Corvallis, cate pots were used for each saline treatment OR). Results of growth, ion contents, net CO2 group, and pots were placed in plastic trays exchange rate, water potential, and stress were containing half-strength Hoagland’s nutrient analyzed with a 3-way ANOVA to determine if solution. All pots were watered immediately significant differences were present among 190 WESTERN NORTH AMERICAN NATURALIST [Volume 60 means. A Bonferroni test determined whether creased with increased density, but there was significant (P < 0.05) differences occurred be- no density effect at higher salinities (Fig. 2). tween individual treatments (SPSS 1996). A 3-way ANOVA showed a significant indi- vidual effect of salinity (P < 0.05) and shoots- RESULTS roots (P < 0.001), while density was not signif- icant in affecting succulence. Interactions be- A 3-way ANOVA showed significant indi- tween density and plant part were significant. vidual effects of plant density, salinity, plant Shoot tissue water showed significant increase part, and their interactions on dry mass of A. at 400 mM NaCl compared to 0 mM NaCl. At occidentalis plants. Interactions between den- high densities (4000 and 6000 plants m–2) and sity and salinity and among all factors were all other salinities, the effect was not signifi- not significant. Dry mass of shoots at low den- cant (Fig. 3). At low planting density, root suc- sity (2000 plants m–2) was not affected by low culence was higher except for 1000 mM NaCl, salinities (200 and 400 mM NaCl; Fig.1). There where at high density there was a substantial was a significant (P < 0.001) promotion in increase in succulence. A 3-way ANOVA shoot growth at 600 mm NaCl (Fig. 1). Shoot showed a significant (P < 0.0001) effect of var- growth at 1000 mM NaCl was not significantly ious concentrations of NaCl on net photosyn- different from the nonsaline control at medi- thesis, water potential, and Fv/Fm ratio. Net um density. At high seedling density (6000 photosynthesis was higher at 200 mM NaCl plants m–2), there was no significant differ- and then significantly declined with increased ence in shoots among various salinity treat- salinity (Table 1). Water potential progressively ments (Fig. 1). As density increased, shoot decreased with increasing salinity, reaching growth progressively decreased at all salinity –6.7 MPa at 1000 mM NaCl. The Fv/Fm ratio treatments. Root growth at low density and declined with increasing salinity. 200 mM salinity was similar to 0 salinity (Fig. A 3-way ANOVA showed significant indi- 2). Salinity ≥600 mM generally decreased dry vidual effects of shoots-roots, salinity, density, mass of roots. At low salinity, dry mass de- and their interaction in affecting ion content

Fig. 1. Effect of NaCl (0, 200, 400, 600, 800, and 1000 mM) on dry mass of shoots of Allenrolfea occidentalis plants –2 –2 –2 ± grown at low (2000 m ), medium (4000 m ), and high (6000 m ) plant density. Bar represents mean sx–. Different let- ters above bars represent significant differences (P < 0.05) among treatments. 2000] PHYSIOLOGICAL RESPONSES OF ALLENROLFEA OCCIDENTALIS 191

Fig. 2. Effect of NaCl (0, 200, 400, 600, 800, and 1000 mM) on dry mass of roots of Allenrolfea occidentalis plants –2 –2 –2 ± grown at low (2000 m ), medium (4000 m ), and high (6000 m ) plant density. Bar represents mean sx–. Different let- ters above bars represent significant differences (P < 0.05) among treatments. of A. occidentalis. Sodium content in shoots cretica showed optimal growth at 425 mM increased at lower salinity, but a further in- NaCl, and there was no inhibition of growth at crease in salinity had no effect (Table 2). 850 mM NaCl. Great Basin Desert species Change in density had little effect on shoot collected from similar habitat, i.e., Salicornia Na+ concentration. Chloride concentration pro- rubra, S. utahensis, Suaeda moquinii, Kochia gressively increased with increases in salinity, scoparia, and Sarcobatus vermiculatus, also but change in density had no effect (Table 2). showed optimal growth at or above seawater Tissue concentrations of Ca–2, Mg–2, K+, salinity (Khan, Gul, and Weber unpublished – –2 NO3 , and SO4 were very low in compari- data). Allenrolfea occidentalis appears to be son to Na+ and Cl–, and they decreased with one of the most salt tolerant species reported. increases in salinity (Table 2). Root ion concen- Increased competition caused a progressive trations followed a pattern similar to that of reduction in growth of A. occidentalis. High the shoot (Table 3). planting density decreased growth even at low salinities. At higher planting densities there DISCUSSION was no significant difference in growth among various salinity treatments. Intraspecific com- Allenrolfea occidentalis showed optimal petition may affect biomass production, repro- shoot growth at seawater salt concentration duction, survival, and growth of halophytes in and higher (600–800 mM NaCl). Most halo- saline habitats (Badger and Ungar 1990, Ungar phytes show optimal growth in the presence 1991, Federaro and Ungar 1997, Keiffer and of salt (Naidoo and Rughunanan 1990, Rozema Ungar 1997). Keiffer and Ungar (1997) reported 1991, Ayala and O’Leary 1995); however, most that such species as Salicornia europaea, halophytic species are inhibited by high salt Atriplex prostrata, Hordeum jubatum, and concentration, with none showing optimal Spergularia marina produce plants of similar growth at seawater concentration (Ungar 1991). biomass under all salinities when grown in Khan and Aziz (1998) reported that Cressa higher density treatments. Keddy (1981) 192 WESTERN NORTH AMERICAN NATURALIST [Volume 60

Fig. 3. Effect of NaCl (0, 200, 400, 600, 800, and 1000 mM) on shoot and root water content of Allenrolfea occidentalis –2 –2 –2 ± plants grown at low (2000 m ), medium(4000 m ), and high (6000 m ) plant density. Bar represents mean sx–. Differ- ent letters above bars represent significant differences (P < 0.05) among treatments. reported the relative importance of density- to contribute to salt regulation by increasing dependent and density-independent effects the vacuolar volume available for ion accumu- can change along environmental gradients. lation (Greenway and Munns 1980, Albert To avoid toxic effects of salt, halophytes 1982, Ungar 1991). Salinity increased the water have developed a number of mechanisms, content of Suaeda torreyana (Glenn and O’Leary including succulence, salt exclusion, and 1984), Salsola kali (Reimann and Breckle secretion (Ungar 1991). Succulence is thought 1995), and Arthrocnemum fruticosum (Eddin 2000] PHYSIOLOGICAL RESPONSES OF ALLENROLFEA OCCIDENTALIS 193

TABLE 1. Effect of salinity on net photosynthesis, midday water potential, and Fv/Fm ratio of Allenrolfea occidentalis.

NaCl Net photosynthesis Water potential Fv/Fm (mM) (µmol m–2 s–1) (–Mpa) ratio 0 9.8 ± 0.6 –3.1 ± 0.3 0.74 ± 0.02 200 12.4 ± 0.6 –3.4 ± 0.3 0.68 ± 0.02 400 7.3 ± 0.7 –4.1 ± 0.2 0.61 ± 0.01 600 6.1 ± 0.7 –4.4 ± 0.6 0.71 ± 0.04 800 7.7 ± 1.1 –4.9 ± 0.2 0.64 ± 0.01 1000 7.4 ± 0.4 –6.7 ± 0.4 0.53 ± 0.03

and Doddema 1986), with this increase in suc- growing at optimal salinity. Differences in culence presumably being a result of salt accu- photosynthetic rates were not consistent with mulation. However, our results showed a sig- differences in growth (Ayala and O’Leary nificant increase in salt accumulation, but a 1995). Our results indicate a small promotion significant reduction in succulence, at higher of photosynthesis at low salinity, while all salinity and plant density. Roots showed a other treatments showed similar effect. clear increase in water content over the entire Changes in Fv/Fm were more evident when salinity range, except at 1000 mM NaCl in A. occidentalis was treated with 1000 mM low-density treatments. Species with succu- NaCl. Low Fv/Fm values were found in the lent leaves (Salicornia europaea, Allenrolfea control and low-salinity treated plants, although occidentalis, and Batis maritima) show a remark- lowest values logically appeared in higher salt able degree of dehydration when treated with treatments. Sharma and Hall (1998), Larcher high (720 mM NaCl) salinity (Glenn and et al. (1990), and Jimenze et al. (1997) also O’Leary 1984). A progressive accumulation of reported similar reduction in Fv/Fm values. At salt with increase in salinity was found. high salinity (1000 mM NaCl) A. occidentalis In dicotyledenous halophytes, water rela- plants showed a slight decrease in mean tions and the ability to adjust osmotically are Fv/Fm values, but this variation could not be reported to be important determinants of the attributed to salinity stress alone (Brugnoli growth response to salinity (Flowers et al. and Lauteri 1990, 1991, Brugnoli and Björk- 1977, Munns et al. 1983, Ayala and O’Leary man 1992). 1995). Our results indicate that water poten- A tendency to accumulate NaCl has been tials of plants reflect osmotic potentials of ex- reported for many other halophytes and is ternal solutions, especially at higher salinities. associated with salt tolerance (Storey and Wyn Allenrolfea occidentalis adjusted osmotically, Jones 1977, Greenway and Munns 1980, maintaining a more negative water potential. Glenn and O’Leary 1984, Naidoo and Rughu- Antlfinger and Dunn (1983) found that species nanan 1990, Nerd and Pasternak 1992, Khan growing in higher soil salinities had a lower and Aziz 1998). Total concentration of inor- xylem pressure potential than plants growing ganic ions in A. occidentalis plants increased in less saline areas. with salinity; this increase is due primarily to Growth inhibition under saline conditions an increase in the concentration of Na+ and is usually associated with dehydration at high Cl–. These 2 ions also contributed substan- salinity, which is due to increased water stress tially to the dry mass content of plants. At all and the resultant loss of cell turgor because of salinities A. occidentalis maintained Na+ con- inadequate tissue osmotic adjustment (Helle- centrations higher than external solutions. bust 1976, Ungar 1991). One major difference Allenrolfea occidentalis plants grew poorly in between plants grown at different salinities the absence of NaCl; optimum growth occurred was photosynthetic response. In supraoptimal at 180–540 mM NaCl and was inhibited by salinity conditions, plant growth was accompa- 40% at 720 mM NaCl compared with 320 mM nied by reduced photosynthetic rates. In sub- NaCl, similar to that for Atriplex canescens optimal salinity conditions, similar growth (Glenn and O’Leary 1984). In shoots and roots reduction was accompanied by photosynthetic of A. occidentalis, increasing salinity signifi- rates equal to or greater than those of plants cantly reduced potassium content. Sodium 194 WESTERN NORTH AMERICAN NATURALIST [Volume 60 . – x s 3 a a a a a a 46 29 28 25 27 17 ± 16 ± 18 ± 9 ± 6 ± 14 ± 6 NO (mM) b a a a c c 50 178 87 83 41 25 ± 5 ± 14 ± 7 ± 26 ± 16 ± 8 a a a b c c 331 334 337 262 171 152 ± 15 ± 44 ± 77 ± 76 ± 8 ± 29 a b c c d d 4 722 426 275 212 181 137 ± 170 ± 93 ± 71 ± 16 ± 18 ± 17 SO (mM) a b a c c d 280 338 263 133 136 146 ± 13 ± 80 ± 28 ± 11 ± 34 ± 29 c c d e a b ± 340 ± 662 ± 147 ± 834 ± 1811 ± 2192 1845 9742 11337 12061 12437 a b c d e – Cl (mM) 2121 ± 105 1088 ± 174 1472± 577 11130 1619 ± 343 4029 ± 170 6096 ± 497 a b c d e e 1616 ± 213 6290 ± 640 6833 ± 874 7161 ± 137 8881 ± 776 8885 ± 343 at low (L), medium (M), and high (H) densities. Values represent means ± at low (L), medium (M), and high (H) densities. Values a a a a a a ntalis e ± 7 ± 8 ± 10 ± 5 ± 7 ± 8 360 340 306 281 269 217 id a b b b b b 2+ a o cc ± 25 ± 32 ± 3 ± 4 ± 21 ± 23 267 175 154 160 148 138 (mM) Mg a a a a b b nrolf e e ± 10 ± 24 ± 15 ± 9 ± 13 ± 11 395 394 339 304 276 257 < 0.05) according to Bonferroni test. All P b a a a a a ± 6 ± 8 ± 34 ± 7 ± 7 ± 8 44 49 117 46 23 13 a b b b b b 2+ ± 24 ± 2 ± 19 ± 6 ± 14 ± 16 109 61 81 96 39 34 Ca (mM) b a a a a a ± 6 ± 68 ± 17 ± 6 ± 1 ± 5 78 145 85 56 26 25 a a a a a a ± 4 ± 2 ± 1 ± 2 ± 5 ± 4 48 40 28 25 23 22 a a a a a a + ± 12 ± 4 ± 5 ± 3 ± 5 ± 12 38 22 27 26 24 23 K (mM) a a a a a a ± 6 ± 3 ± 12 ± 4 ± 3 ± 4 52 42 28 30 31 35 a b c c c c ± 97 ± 198 ± 745 ± 71 ± 141 ± 61 + Na 1671± 486 1296 4859± 88 4539 5303± 99 5122 5655± 109 5484 5464± 165 5541 5742± 272 5607 a b c c c c MLHMLHLMH LMHLM LMHLMHLMHLMH 2. Effect of salinity on the concentration cations and anions in shoots ± 86.2 ± 153 ± 274 ± 29 ± 66 ± 224 ______ABLE T NaCl (mM)0 (mM) 1270 Means in same column followed by the letter are not significantly different ( 200 4434 400 5218 600 5272 800 5284 1000 5392 2000] PHYSIOLOGICAL RESPONSES OF ALLENROLFEA OCCIDENTALIS 195 . – x s ± 3 a a a ab b b 98 57 56 30 21 19 ± 20 ± 9 ± 10 ± 2 ± 1 ± 5 NO (mM) a a a a a a 39 43 34 30 28 24 ± 12 ± 18 ± 12 ± 6 ± 12 ± 8 a a b c d d 764 739 596 470 305 142 ± 22 ± 23 ± 17 ± 18 ± 10 ± 18 a a a a a a 4 277 269 281 262 251 211 ± 55 ± 13 ± 7 ± 12 ± 18 ± 9 SO (mM) a b c c d d 844 648 499 431 304 205 ± 26 ± 69 ± 9 ± 11 ± 13 ± 19 a b a c d d ± 55 ± 193 ± 205 ± 356 ± 357 ± 326 1988 1279 2395 5300 5918 d e e a b – Cl (mM) 1899 ± 238 6204 ± 183 9237± 169 1988 12189 ± 782 13864 ± 976 13789 ± 744 a a a a b c 1732 ± 113 1783 ± 100 1837 ± 175 1886 ± 124 2990 ± 726 6963 ± 486 at low (L), medium (M), and high (H) densities. Values represent Means at low (L), medium (M), and high (H) densities. Values a a a a a a ± 24 ± 8 ± 13 ± 8 ± 7 ± 11 226 195 186 185 174 150 a a a a a a 2+ ± 24 ± 6 ± 15 ± 12 ± 13 ± 11 356 344 352 343 306 283 (mM) Mg < 0.05) according to Bonferroni test. a a a a b b P ± 21 ± 19 ± 13 ± 14 ± 17 ± 3 179 174 150 131 116 96 Allenfolfea occidentals a a a b b b ± 15 ± 8 ± 12 ± 9 ± 12 ± 9 112 104 95 69 66 43 a b c c c c 2+ ± 78 ± 6 ± 8 ± 2 ± 2 ± 5 222 158 87 81 73 45 Ca (mM) a a ab b b b ± 13 ± 9 ± 4 ± 6 ± 5 ± 8 107 99 63 46 45 39 a a a a a a ± 3 ± 4 ± 1 ± 2 ± 2 ± 2 26 20 18 18 17 16 a a a a a a + ± 4 ± 2 ± 2 ± 2 ± 1 ± .09 51 36 33 31 26 24 K (mM) a a a a a a ± 6 ± 2 ± 4 ± 1 ± 3 ± 2 22 21 18 16 14 a b c c c ± 57 ± 43 ± 499 ± 124 ± 141 ± 631 1891 5290 5848 5978 5909 16 5997 a b c c c c + Na 2084 ± 166 4996 ± 93 5557 ± 196 5580 ± 221 5598 ± 140 5738 ± 84 a b c c c c MLHMLHLMH LMHLM LMHLMHLMHLMH 3. 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