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Keywords:

  • Abies lasiocarpa;
  • alpine–treeline ecotone;
  • Cenococcum geophilum;
  • conifer seedlings;
  • ecophysiology;
  • ectomycorrhizas;
  • Picea engelmannii

Summary

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References
  • • 
    Plants establishing in environments that are marginal for growth could be particularly sensitive to mycorrhizal associations. We investigated ectomycorrhizal colonization and its significance for young conifers growing at, or above, their normal limits for growth, in the alpine–treeline ecotone.
  • • 
    Colonization of seedlings (< 1 yr old) and juveniles (2- to 10-yr-old) of Picea engelmannii and Abies lasiocarpa by Cenococcum geophilum was determined in a field study, and effects of Cenococcum on Picea seedling ecophysiology were investigated in a glasshouse.
  • • 
    Colonization by Cenococcum was c. 20-fold greater for juveniles than seedlings, and ~4-fold greater adjacent compared with ~7 m away from trees. Juveniles of Picea were more colonized at timberline than Abies, and the opposite relationship was observed in forest. Colonization enhanced seedling water potential, but not phosphorus concentrations or photosynthesis.
  • • 
    These landscape and age-dependent variations in colonization correspond well with known variations in conifer physiology and establishment near timberline. Facilitation of seedling establishment by older trees at alpine–treeline may include a below-ground, mycorrhizal component that complements previously reported effects of trees on the microclimate and ecophysiology of seedlings.

Introduction

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References

Ectomycorrhizal associations of fungi and plant roots are widespread in subalpine and subartic forest (Read, 1991; Gardes & Dahlberg, 1996). Ectomycorrhizal fungi receive carbon from host plants, and can deter root pathogens and enhance nutrient and water relations for host plants (reviewed in Smith & Read, 1997). The balance of costs and benefits of fungal symbionts may differ for plants in stressful compared with in more amenable, temperate, or agricultural conditions. A better understanding of the role of ectomycorrhizas for plants establishing in marginal growth conditions could yield important insights on the general importance of mycorrhizas. Young conifers establishing at the upper altitudinal limits of their species range, in subalpine meadows, experience limitations to carbon assimilation (Germino & Smith, 1999, 2000; Johnson et al., 2004) and might therefore be more critically affected by mycorrhizal associations than plants in other habitats. Factors affecting survival of conifers in their first few years of growth appear important for conifer populations at high elevations, based on high mortality rates for the youngest seedlings (Germino et al., 2002).

The alpine–treeline ecotone (ATE) is the transition zone from closed-canopy forest to treeless, alpine meadows. Trees at the ATE experience greater climatic stress than those at lower elevations (Korner, 1998; Smith et al., 2003). In many Rocky Mountain ATEs, tree species of Picea, Abies, and Pinus often occur in clusters, or ‘tree islands’, which are interspersed by alpine tundra. Establishment of young conifers in such ATEs appears greater near tree islands (Germino et al., 2002). Tree islands ameliorate harsh climatic conditions such as frost, strong sunlight, desiccation, and snow cover for seedling microsites in the ATE, which in turn, appear to enhance the photosynthetic physiology of young conifer seedlings and thereby facilitate their establishment (Germino & Smith, 1999; Germino et al., 2002; Smith et al., 2003). Soil physical and chemical properties, however, are also modified by tree islands (Holtmeier & Broll, 1992; Pauker & Seastedt, 1996; Van Miegroet et al., 2000). Greater establishment under adult trees in the ATE could also be due to below ground mechanisms of facilitation, such as those involving mycorrhizas described for low-elevation forests (Dickie et al., 2002).

The ectomycorrhiza Cenococcum geophilum Fr. is frequently encountered in the field (Horton & Bruns, 2001), especially in forests and at alpine–treeline (Kernaghan & Harper, 2001). The objective of this research was to determine the role of colonization of young conifers by C. geophilum in the ATE. We hypothesized that: (i) colonization would vary similar to how survival and carbon assimilation differed among plant developmental stages and among microsites with different levels of tree cover, as described in Germino & Smith (1999) and Germino et al. (2002); and that (2) C. geophilim would enhance carbon, water, and nutrient relations of young conifers. Measurements of photosynthetic CO2 uptake may detect even minor fitness gains that result from mycorrhizal colonization and could enhance survival of seedlings in marginal ATE environments. Water and nutrient relations of seedlings were measured because mechanisms by which C. geophilum could enhance photosynthesis were expected to involve increases in soil resource uptake. We refer here to conifers in the first year of growth as seedlings, and to those aged 2- to 10-yr-old as juveniles. Colonization by C. geophilum was measured along transects spanning the gradient from forest to alpine, for naturally occurring seedlings and juveniles. Additionally, a glasshouse study was conducted to investigate the functional significance of C. geophilum for host P. engelmannii seedling physiology. Information concerning the occurrence and functional benefits of C. geophilum on young conifers across the ATE may lead to a better understanding of the general importance ectomycorrhizal fungi play in the facilitation of seedling establishment by trees in stressful environments.

Materials and Methods

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References

Geographic locations and tree species

Study sites were located within the ATE of the Snowy Range in south-east Wyoming (41°20′30″ N 106°14′30″ W) and the Beartooth Mountains in north-central Wyoming (45°01′59″ N 109°24′21″ W). The climate for both mountain ranges is characterized by cold winters from September to June with minimum annual air temperatures from −25 to −40°C. Summers typically have daily maximum air temperatures below 25°C with frequent clear skies and nocturnal frost. Much of the annual precipitation comes during winter as snow, and snowbanks frequently persist into August. Two codominant conifer species, Picea engelmannii Parry and Abies lasiocarpa (Hook.) Nutt., occur in islands interspersed among alpine tundra within the ATE.

The ATE consists of three zones: forest, timberline, and treeline. At timberline, trees of mature stature form a patchy mosaic of tree islands. Treeline is the upper limit of tree growth, where trees are also in tree islands but are severely reduced in growth with krummholz morphology. No conifer seedlings or juveniles were found at treeline, and we therefore limited our field study to conifers found in the forest and at timberline.

Seedling occurrence and percent colonization

The frequency of C. geophilum colonization was measured for all naturally occurring P. engelmannii and A. lasiocarpa seedlings and juveniles found at our study sites. Seedlings were distinguished from juveniles based on the presence of cotyledons and primary needles, and wood formation in stem. In 2002, measurements were made on 101 juveniles found along transects of 2 m width and 30 m length, which were positioned in representative areas of forest and timberline zones of each mountain range (n = 3 per life zone). Additionally, the distance to the nearest adult tree was measured for each juvenile found at timberline. No first-year seedlings were detected in 2002, however, 83 conifer seedlings were found in 2003 along two transects that traversed the forest and timberline life zones in the ATE of the Snowy Range (N = 2 transects per life zone).

Root systems of young conifers were carefully excavated from the soil, gently washed with water to remove soil debris, and stored in 70% ethanol. All root lengths were later examined for the presence of fungal colonization under 40× magnification. Cross sections of colonized root tips were examined for the presence of hartig nets, and colonization levels were calculated for individual conifers as the percent of root tips colonized. All fungi that formed mantles and hartig nets on roots of our subject plants had the distinctive morphological features of C. geophilum (e.g. Goodman et al., 1996; Hagerman et al., 1999; Agerer, 2002). Roots of older conifers near our younger subject plants appeared to have a much higher diversity of black and ectomycorrhizal fungi, as revealed by morphological and molecular assessments (Hasselquist et al., unpublished data). Our study focused on C. geophilum because all other fungal species we observed on roots were not ectomycorrhizal. Any other ectomycorrhizal species that may have been present on roots of subject plants, but were not detected, would have had very small abundances.

Glasshouse study

Seeds of P. engelmannii were sterilized in 30% H2O2 for 10 min, rinsed three times with deionized water, and then placed into 20 cm × 20 cm × 1 cm Plexiglass microcosms. These microcosms were filled with a commercial organic potting mixture (FertiLome, Voluntary Purchasing Groups Inc., Bonham, TX, USA) that was pasteurized at 80°C for 4 h in a soil sterilizer (model SST-60R, Pro-grow Supply Corp., Brookfield WI, USA). Soil in the microcosms was shaded from light to inhibit algal growth. Following germination, approx. 1 cm3 of agar that either contained C. geophilum or was sterile (control group) was placed within 1 cm of seedling roots in each microcosm (n = 14 per treatment) and grown for two months to ensure fungal colonization, which was verified visually.

All 28 seedlings were later transplanted individually into 400 ml pots containing a sterilized sandy loam with a pH of 7.2 and a bulk density of 1.4 g cm−3. Volumetric soil water content was monitored gravimetrically and maintained near 0.20 m3 H2O m−3 soil with daily additions of distilled water. Approx. 72 mg of nitrogen as aqueous ammonium nitrate was initially added to each pot. Transplanted seedlings were placed under a 16 h: 8 h (day: night) photoperiod generated by natural sunlight and two 400-watt metal halide lamps (G3400-1G+, Rudd Lighting Inc., Racine, WI, USA), which generated maximum photon flux densities near 1000 µmol m−2 s−1 (400–700 nm). Air temperatures ranged diurnally from 10 to 25°C. After 6 wk of growth, daily watering stopped and photosynthesis measurements began for four consecutive days, during which volumetric soil water content decreased from 0.20 to 0.068 m3 H2O m−3 soil. Destructive measurements of water status, biomass, and nutrient concentrations were performed on the fourth day following cessation of watering. Volumetric soil water content was determined gravimetrically each day as the soils were allowed to dry (n = 28).

Photosynthesis was measured on P. engelmannii seedlings for each of the 4 d soils were allowed to dry (n = 7 for colonized seedlings and n = 14 for noncolonized seedlings). Instantaneous photosynthetic carbon assimilation rates (A), transpiration (E), and water use efficiency (WUE = A/E) were measured with a closed-flow gas exchange system (LI-6400, Li-COR Biosciences, Inc., Lincoln, NE, USA) equipped with a light source. Readings were taken at ambient CO2 levels (approx. 370 ppm), at a light level of 1000 µmoles m−2 s−1, and at temperatures near 27°C. Measurements were made on entire seedlings, and reported on a silhouette leaf area basis, which is the amount of leaf area perpendicular to, or illuminated by the artificial light source in the chamber of the LiCOR 6400. Leaf areas were determined by photographing seedlings from the angle in which they were illuminated during measurements, with objects of known size in the field of view (model Coolpix 990, Nikon, USA). Leaf areas in the resulting digital image were then determined using image-processing software (Image J, Scion Image, Frederick MD, USA).

Xylem water potential were measured for all seedlings using a Scholander-type pressure chamber (model 1000, Plant Moisture Stress, Corvallis, OR, USA). Root systems were carefully harvested and thoroughly rinsed, and examined under 40× magnification to determine the percent of root tips colonized by C. geophilum. Biomass of roots and shoots were measured to the nearest tenth of a milligram at the end of the experiment, following 24 h of drying at 80°C. Phosphorus concentrations were determined by first digesting each entire seedling in a 10 : 1 nitric acid : sulfuric acid mixture using the method of Hall (1995), and then measuring absorbance at 880 nm using an auto-analyzer after reacting the resulting orthophosphate with molybdenum in the presence of antimony in sulfuric acid, using the manufacturer's methodological specifications (for Standard Methods of US Environmental Protection Agency; Alpken FS 3000, OI Analytical, College Station, TX, USA) at the Center for Ecological Research and Education at Idaho State University.

Statistical analysis

Chi-square analysis was performed to determine if there was a significant difference in the relative abundance of conifer species between the forest and timberline life zones. Because of the low degrees of freedom associated with the data sets (d.f. = 1), we used the Yates correction for continuity while performing the chi-square analysis (Zar, 1999). One-way analyses of variance (anova), followed by Tukey tests (α < 0.05) for mean separation (Zar, 1999, JMP Version 3.2.2., SAS Institute, Cary, NC, USA), were employed to detect significant differences in C. geophilum colonization between conifers species (P. engelmannii and A. lasiocarpa) and between each life zone (forest and timberline). Least-squares regression analysis was used to investigate the correlation between C. geophilum colonization levels at timberline and the distance to nearest adult tree. One-way anova was also used to detected differences in physiological measurements between colonized and noncolonized seedlings. Regression analysis was used to determine correlations between the percent of root tips colonized and measurements of host conifer physiology.

Results

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References

Seedling occurrence and colonization

Only three of the 83 first-year seedlings we found were colonized by C. geophilum. All three seedlings were A. lasiocarpa and were found in the forest. In contrast, 52% of all conifer juveniles were colonized by C. geophilum, with mean ± se colonization levels of 39 ± 3.5%. The percent of conifer juveniles colonized by C. geophilum was not significantly different between the forest and timberline life zones or between the two conifer species. However, an important interaction emerged between conifer species and life zone for the percent of juveniles colonized by C. geophilum (F3,10 = 7.55, P = 0.03). Among juveniles, 71 ± 4% of A. lasiocarpa and 52 ± 18% of P. engelmannii were colonized by C. geophilum in the forest, whereas 17 ± 17% of A. lasiocarpa and 67 ± 10% of P. engelmannii were colonized at timberline. We also noted that A. lasiocarpa was twice as abundant as P. engelmannii among juveniles in forest, and P. engelmannii was more than 10-fold more abundant than A. lasiocarpa at timberline (χ2 = 69.02, P < 0.01). No significant differences in the relative abundance of first-year conifer seedlings were detected between these two life zones. At timberline, the percent of root tips colonized by C. geophilum was c. 4-fold greater for seedlings located within c. 1 m compared with 7–8 m away from adult trees (F1,58 = 4.37, P = 0.04, Fig. 1), although a r2 = 0.07 indicated that other sources of variation in colonization were important but not identified.

image

Figure 1. Correlation between the percent of juvenile root tips colonized by Cenococcum geophilum and distance to nearest adult tree for all juveniles found at timberline in both the Snowy Range (south-east Wyoming, USA) and Beartooth Mountains (north-central Wyoming). n = 59.

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Glasshouse study

Colonization of inoculated P. engelmannii roots by C. geophilum ranged from 3 to 54% of root tips, with an average of 25 ± 3.8% of root tips. Following cessation of watering, there was a significant decrease in volumetric soil water content from 0.20 ± 0.001 to 0.068 ± 0.001 m3 H2O m−3 soil from the first to the last of the 4 d of drying, respectively (F3,38 = 6511.09, P < 0.01).

No significant differences in mean A or WUE were detected between colonized and noncolonized seedlings on individual days or across days of the dry-down period. Mean A was similar for colonized and uncolonized seedlings from days one (2.45 ± 0.06 and 2.50 ± 0.07 µmol m−2 s−1, respectively) to day three following cessation of watering, with A decreasing from c. 2.5–2.0 µmol m−2 s−1 during the period for both treatment groups. By the fourth and final day of drying, there was still no significant difference in mean A in colonized (0.75 ± 0.70 µmol m−2 s−1) compared with uncolonized seedlings (0.41 ± 0.65 µmol m−2 s−1). WUE was 0.49 ± 0.01 and 0.50 ± 0.01 µmol mmol−1 for colonized and uncolonized seedlings, respectively, on day one, and remained statistically similar during the experiment. However, higher levels of C. geophilum colonization were associated with less negative seedling water potentials (F1,9 = 4.85, P = 0.06, Fig. 2). Total biomass was not significantly different between colonized and noncolonized seedlings. Furthermore, root : shoot ratios were similar for colonized and noncolonized seedlings. Plant tissue phosphorus concentrations ranged from 1.0 to 3.2 mg P g−1 dry tissue and were not responsive to colonization, whether mean P concentrations of seedlings with any level of colonization were compared with uncolonized seedlings (F1,27 = 0.002, P = 0.97) or if P concentrations were compared with percent of root tips colonized by C. geophilum (F1,13 = 1.97, P = 0.18, Fig. 3).

image

Figure 2. Correlation of percent of root tips colonized by Cenococcum geophilum and seedling water potential, measured in a glasshouse. n = 10.

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image

Figure 3. Correlation of seedling phosphorus concentration and the percent of root tips colonized by Cenococcum geophilum, measured in a glasshouse. n = 14 seedlings.

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Discussion

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References

Previous studies reported changes in the composition and abundance of mycorrhizal communities along elevation gradients that also included changes in the species composition of plant communities (Haselwandter & Read, 1980; Read & Haselwandter, 1981; Kernaghan & Harper, 2001). Our study demonstrated that variation in mycorrhizal colonization could also occur for specific conifer species that span elevation gradients encompassing thresholds for conifer growth and survival. Furthermore, the variation in C. geophilum colonization of young conifers reported here corresponds to previous reports of age and microsite-based variation in photosynthesis, survival, and establishment of conifer seedlings.

Age-based variation in colonization

Mortality rates up to 99% have been observed for first-year conifer seedlings near alpine timberline (Cui & Smith, 1991; Germino et al., 2002). In second and subsequent seasons of growth, conifer survivorship appears to increase exponentially, and mortality is rarely observed among 2-yr- or older juveniles. Our finding of very low frequency of C. geophilum colonization on first-year seedlings but nearly 20-fold higher frequencies of colonization for older juveniles is an indirect indication that colonization by C. geophilum may be important for conifer survival in the ATE. Two other studies also reported high frequencies of mycorrhizal colonization on conifer seedlings surviving beyond the initial season of establishment (Christy et al., 1982; Miller et al., 1998), suggesting the potential ecological importance of mycorrhizae for initial survival of conifers in their first season following germination.

Microsite-based variation in colonization

Colonization of juvenile conifers by C. geophilum appeared heterogeneous at timberline (Fig. 1). Juvenile conifers previously appeared much more abundant in microsites adjacent to adult trees, due apparently to low survivorship of emergent seedlings metres away from adult trees (Germino et al., 2002). Correspondingly, we detected a significantly higher level of C. geophilum colonization for conifer juveniles found closer to adult trees compared with away from adult trees.

Adult trees shade microsites for seedling establishment from bright sunlight levels, which can be 30% greater at alpine than at sea-level (Korner, 1998). Furthermore, microsites near adult trees at timberline experience fewer nights with nocturnal frost compared with microsites further away from adult trees, because trees emit more thermal, longwave radiation towards the ground than clear skies at night (Jordan & Smith, 1995). Nocturnal frost followed by high levels of solar radiation can lead to low-temperature photoinhibition and marked reductions in seasonal photosynthesis for young conifers at timberline (Germino & Smith, 1999). Based on the agreement between increased seedling photosynthesis in response to artificial shade and nocturnal warming, Germino & Smith, 1999, 2000; Germino et al., 2002) inferred that greater seedling establishment adjacent to adult trees was due to protection from bright sunlight and radiation frost provided by trees, similar to that detected for Eucalyptus (Ball, 1994).

Our data provides some evidence that greater seedling establishment near adult trees may also result from below-ground mechanisms involving mycorrhizas, such as those described for low-elevation forests (Dickie et al., 2002). Greater colonization of establishing conifers in microsites near adult trees at timberline (Fig. 1) could indicate that adult trees are a source of C. geophilum inoculum for young conifers. Mycorrhizal colonization of young seedlings of other tree species was greater when seedlings were near older individuals that had more extensive levels of colonization (Harvey et al., 1980; Read, 1984; Newman, 1988; Borchers & Perry, 1990; Parsons et al., 1994). Also, mycorrhizal diversity in soil and on conifer roots decreased at distances greater than a few meters from forest edges in clear cuts and gaps in subalpine and hemlock forests of British Columbia (Hagerman et al., 1999; Kranabetter & Wylie, 1998), and trenching between seedlings and adult trees led to significant decreases in the richness and diversity of fungi on seedlings (Simard et al., 1997a). Thus, greater abundances of ectomycorrhizal inoculum could be an important way that establishing conifers located near adult trees develop higher levels of mycorrhizal colonization (Fig. 1).

Variation in colonization among species and life zones

Relatively greater C. geophilum colonization of juveniles of Picea than Abies at timberline, and of Abies compared with Picea in forest, corresponded well with previously reported differences in their relative abundances and photosynthesis in each life zone (Germino et al., 1999). Juveniles of Abies appeared considerably more susceptible than Picea to low-temperature photoinhibition of photosynthesis, and, correspondingly, Abies was relatively less abundant than Picea at timberline than in forest (Germino & Smith, 1999, 2000; Germino et al., 2002). Conversely, photosynthesis was greater in juveniles of Abies compared with Picea in the forest understory, and under experimental conditions of warmer nights and daytime shade at timberline (Knapp & Smith, 1981; Germino & Smith, 1999).

Functional benefits of colonization

Despite strong associations of ectomycorrhizal colonization and photosynthesis and survival between the current and previous studies, colonization by C. geophilum did not appear to lead to greater photosynthesis in our glasshouse experiment. This finding is also in spite of increases in water potentials of colonized seedlings to levels above levels measured for uncolonized seedlings and which previously appeared to cause reductions in photosynthesis of P. engelmannii seedlings (Fig. 2; Johnson et al., 2004). Colonization did not lead to significant phosphorus enrichment of seedlings, which were individually potted (Fig. 3). These glasshouse results must be interpreted with caution because seedlings in the field or potted with older trees might receive carbon or other nutrient subsidies through ectomycorrhizal links to nearby plants (Newman, 1988; Simard et al., 1997b; but see Robinson & Fitter, 1999). Light, temperature, and other factors in the glasshouse also differed from field conditions, and fertilization may have minimized ectomycorrhizal enhancement of plant nitrogen.

Ectomycorrhizas can enhance plant water relations (Duddridge et al., 1980; Parke et al., 1983; Coleman et al., 1990; Nardini et al., 2000), and C. geophilum appears relatively drought tolerant among ectomycorrhizas (Worley & Hacskaylo, 1959; Mexal & Reid, 1973; Piggot, 1982; Coleman et al., 1989). Our data indicated that the benefits of C. geophilum to conifer seedlings may be particularly evident under conditions of water limitation, which is an important stress for plants in the ATE (Smith & Geller, 1979). Greater water potentials without changes in photosynthetic CO2 or H2O exchange for seedlings with greater levels of colonization (Fig. 2), suggest that C. geophilum may be more likely to enhance uptake rather than conservation of water.

Conclusions

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References

Facilitative interactions can become more prevalent compared with competitive interactions among plants in relatively stressful environments, such as at high elevations and in the alpine (Callaway, 1998). Several studies now support a strong facilitative effect of trees on conifer seedling establishment in the ATE (Germino & Smith, 1999; Germino et al., 2002). These previous reports suggested that facilitation occurred through above-ground shading of seedlings by trees, whereas our results indicate that a below-ground mechanism involving mycorrhizae may also mediate tree facilitation of seedlings. Increased availability of inoculum and enhanced microclimate for photoassimilate production appeared to be potential ways that trees could increase ectomycorrhizal colonization of seedlings, which, in turn, is correlated with greater water relations (Fig. 2) and survivorship (Germino et al., 2002). These above- and below-ground mechanisms likely interact in complex ways to affect establishment of conifers beyond their normal or optimal range of suitable growth conditions, at alpine–treeline.

Acknowledgements

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References

Funding was provided by a National Science Foundation Ecology and Evolutionary Physiology grant to WKS and a Mellon Foundation grant to MJG. We thank Eliza Maher and Lisa Marno for field assistance and Brad Thomas of the Center for Ecological Research and Education at Idaho State University for phosphorus determinations.

References

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References
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