Shoot regrowth and age-specific rhizome storage dynamics of Phragmites australis subjected to summer harvesting

Ecological Engineering 22 (2004) 99–111

Shoot regrowth and age-specific rhizome storage dynamics of Phragmites australis subjected to summer harvesting Shiromi Karunaratne1 , Takashi Asaeda∗ , Kentaro Yutani Department of Environmental Science and Human Engineering, Saitama University, 255 Sakura ward, Shimo-okubo, Saitama 338-8570, Japan Received 31 July 2003; received in revised form 24 February 2004; accepted 25 February 2004

Abstract Shoots of a monospecific wetland stand of Phragmites australis (Cav.) Trin. ex Steud. in Central Japan were harvested during two summer months in June (June-cut stand) and July (July-cut stand) and their effects on the stand morphology, above- and below-ground biomass and rhizome storage level (in terms of age-specific rhizome bulk density, ρrhiz ), were investigated between themselves and to an uncut control stand. Both harvesting treatments increased leaf production and decreased shoot height, stem diameter, and the storage accumulation capacity of older rhizome age categories, the June-cut stand showing the lowest ρrhiz . Even though the year-end age-specific rhizome reserve level did not reach to that of uncut stand values, both treatments accelerated the post-harvest rhizome reserve accumulation rates (i.e. rate of ρrhiz increment) stimulated by shoot harvesting, especially in younger rhizomes and were negatively and linearly correlated with rhizome age. The study identified the seasonal changes of the rhizome reserve quality as essential for proper vegetation management. July or August is the appropriate harvesting time for plant stands used in phytoremediation and wastewater treatment, where a larger shoot-bound nutrient stock is removed, while preserving a healthy stand for the subsequent years. A harvest in May to June would be more effective in reducing the growth, and repeated June-cutting may likely weaken the stand beyond repair after several years. © 2004 Elsevier B.V. All rights reserved. Keywords: Biomass; Bulk density; Harvesting; Shoot regrowth; Stand morphology; Rhizome age; Rhizome storage; Translocation

1. Introduction Recent developments in the application of wetland plants for wastewater treatment and phytoremediation for heavy metal removal from soils have gained ∗ Corresponding author. Tel.: +81-48-858-3563; fax: +81-48-858-3563. E-mail address: [email protected] (T. Asaeda). 1 Present address: Department of Earth Resources Engineering, University of Moratuwa, Katubedda, Moratwa, Sri Lanka.

much acceptance world-wide (Brown et al., 1994). Common reed [Phragmites australis (Cav.) Trin. ex Steud.] is one of the commonly used plant species in such applications due to its ability to uptake pollutants and heavy metals such as Cr, Cu, Mn, Zn and petroleum hydrocarbons, etc. (Larsen and Schierup, 1981; Schierup and Larsen, 1981). Harvesting and disposing of shoot biomass, which has extracted target pollutants or heavy metals from soil is the clearest mechanism for permanently managing soil contamination using vegetation.

0925-8574/$ – see front matter © 2004 Elsevier B.V. All rights reserved. doi:10.1016/j.ecoleng.2004.02.006

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On the other hand, P. australis can be a troublesome weed invading various cultures, e.g. rice or cane (Izatt, 1979), fishponds, lakes, and channels (Hellings and Gallagher, 1992), or freshwater wetlands such as fens (Biewer, 1994). This may decrease species richness or cause complete disappearance of typical native species. Different techniques are known for the management/control of P. australis. Traditional methods such as summer or autumn cutting to which the protected species are adopted would be more appropriate in species rich vegetation types (Gusewell, 1998; Husak, 1978). Consequently, many reed stands around the world are managed using different techniques to achieve different goals. The time reeds are harvested strongly influences the regrowth and consequently the effectiveness of harvesting in suppressing or long term survival of P. australis populations. Thus, the effects of summer harvesting of P. australis shoots on seasonal above-ground production and growth dynamics has been the subject of several past studies (Gusewell, 1998; Gryseels, 1989; Weisner and Graneli, 1989; Husak, 1978), while investigations of its effects on both shoot regeneration and rhizome dynamics remain scarce. The storage functions of rhizomes deserve special attention, as they largely determine the stability and survival capacity of the stand. Though some recent studies have reported on rhizome dynamics in relation to water level (Rea, 1996; Weisner and Strand, 1996) and luxury consumption of reserves (Cizkova and Bauer, 1998; Cizkova et al., 1996; Cizkova-Koncalova et al., 1992; Kubin et al., 1994), studies concerning the effects of mid-season mowing and harvesting remain scarce. However, to optimize vegetation management, it is essential to better understand the ecophysiological mechanisms regulating these plant communities and in particular seasonal changes in rhizome biomass and the components contributing to it (Graneli et al., 1992). An extensive and detailed study conducted in a wetland area in central part of Japan in 2000 sought to investigate the effects of summer harvesting on the regrowth dynamics of P. australis and in particular, on age-specific rhizome storage dynamics of P. australis. Rhizome bulk density (ρrhiz ) and chemical characterization of rhizome-bound carbohydrates are often utilized as indicators of storage reserve level of rhizomes of P. australis and other similar species (Midorikawa

et al., 1963; Mutoh et al., 1968; Fiala, 1976; Graneli et al., 1992; Kubin et al., 1994; Klimes et al., 1999). Karunaratne et al. (in press-ab) showed that ρrhiz was fairly representative of rhizome total non-structural carbohydrate (TNC) content. Therefore, ρrhiz , an easily measurable parameter and a good indicator of the seasonal rhizome storage reserve content was selected to study the relationship between reserve accumulation/remobilization and age of P. australis rhizomes. The effects on both the above- and below-ground stand parts from cutting in June, when the shoot growth is rapid and storage reserves in rhizomes are near the seasonal minimum, was compared with cutting in July, when shoot growth is slower and rhizomes reserves are being recharged. The study sought to address the following questions: how do the two cutting regimes affect: (i) shoot morphology during the regrowth phase of P. australis? (ii) age-specific ρrhiz and their by the seasonal storage pattern and resource allocation mechanisms of P. australis rhizomes during the regrowth stage? The study also investigated the management implications of the different harvesting regimes.

2. Methods and materials 2.1. Study site The study was conducted in a wetland portion of ◦ ◦ Akigase Park (35 51 N, 139 39 E) located on the flood plain of Arakawa River in central part of Japan. The study site was dominated by a homogeneous monospecific stand of P. australis covering more than 1000 m2 , and undisturbed over the last 20 years. During the investigations in 2000, water depth on sampling days varied between 0.5 m below and 0.2 m above the soil surface. Though waterlogged conditions did not last for long periods after heavy seasonal rains, from July to November the water level always remained very near or above-ground level. The substrate was soft brown organic loam, 40 cm deep overlying hard clay, thus more than 95% of the rhizome system was contained within the top 40 cm. Considering the uniform topography of the study area (slope <0.5%) and the homogeneity of the P. australis stand, total area was divided into three plots

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of roughly equal area (each plot  10 m × 50 m) adjoining each other in order to minimise the edge effects and disturbances due to trampling during a season long sampling programme. One plot remained uncut throughout the observation period (control plot or “uncut stand”), another plot was cut on 4 June (June-cut stand) and the remainder was cut on 4 July (July-cut stand). With hedge clippers all the shoots were cut at 0.25–0.30 m above-ground level so that no leaf blades were present on the remaining stubble and the harvested shoots removed from the study area immediately. The allowance from the ground level to the cutting level was maintained to prevent the complete inundation of stalks (and resultant rotting) immediately after cutting, during the rainy season. 2.2. Sampling A roughly monthly sampling programme with three quadrats per treatment, resulting in nine samples per sampling day, was implemented. Representative samples were taken to cover the length-wise direction ( 50 m), covering the two ends and middle area. Plant samples were harvested on 3, 19, and 28 April (onset of spring shoot growth), 10 May, 4 June, 4 and 18 July, 1 August, 9 and 18 September, and 24 October 2000. On 19 April, 4 July and 9 September, only the above-ground biomass was sampled. Further, on 28 April, 18 July, and 18 September, below-ground biomass was sampled only for ρrhiz measurements. Sampling for rhizome biomass measurements in July and September was impossible due to elevated water levels caused by the seasonal rains. Shoots were harvested over an area of 0.125 m2 and rhizomes and roots were excavated, with a garden spade, up to a minimum depth of 0.6 m under the same area where the shoots were harvested. Methods of sample analysis for morphology, aboveand below-biomass and bulk density followed same protocols as previous studies done at the same site by Karunaratne et al. (in press-ab). In addition, after summer harvesting in June- and July-cut stands, the nature of re-shooting was recorded. In the harvested stands only newly sprouted shoots were included in the measurements, not the stubble which might have varied among the subsequently sampled quadrats.

101

2.3. Rhizome dating and bulk density Identification of rhizome age categories was based on: (i) the position in branching hierarchy; (ii) condition of the shoots attached to vertical rhizomes: live green shoots are attached to 1-year-old rhizomes, dead shoots are attached to older rhizome material; (iii) condition of the nodal sheaths: intact and tightly covered in newly-formed rhizomes, loosely attached or partly disintegrated in 1–2-year-old rhizomes and absent in rhizomes over 3-year-old; and (iv) colour (which becomes darker with age). Rhizomes of up to 6 years of age were identified. On each sampling date, ρrhiz of some 35–40 intact internodes from each age category from each stand was measured. A detailed description of the rhizome age identification and bulk density measurement are given in Karunaratne et al. (in press-ab). During October sampling, bud formation details such as spatial bud density, bud diameter and specific bud weight (dry weight/fresh length) were measured on buds >5 mm (these were considered to be the potential buds for the following growing season) in all the three blocks. 2.4. Statistics Differences in ρrhiz among the age classes during a sampling date were analyzed using one-way analysis of variance (one-way ANOVA). During June and October samplings, differences in the age-specific ρrhiz among the three treatments were analyzed using two-factor analysis of variance (two-way ANOVA). Differences in the seasonal course of age-specific ρrhiz variation among the treatments were evaluated using three-factor analysis of variance (three-way ANOVA) with Tukey’s multiple comparison as a post-test. Bartlett’s test was used to test the homogeneity of variances. An unpaired t-test was used to evaluate the differences between two independent means. The differences between the single values were assessed using 95% confidence intervals for means.

3. Results From April to their respective cutting times if any, all the three stands (uncut, June- and July-cut) showed no significant differences (P > 0.05) in growth char-

Stem diameter after shoot harvesting refers strictly to the diameter of the stems regenerated from buds (mean ± standard error). Ax. branches: axillary branches.

1 ± 0.02 – 3 ± 0.4 – 7 ± 2.19 – 10 ± 0.5 – 10 ± 1.1 – 1 ± 0.37 – 72 ± 6 –

5.67 ± 0.2 –

4.19 ± 0.1 – 99 ± 6 11 ± 2 96 ± 4 – From buds Ax. branches 24.10.2000

4.83 ± 0.2 –

– – 1 ± 0.5 – 8 ± 0.64 – 5 ± 0.4 – 6 ± 1.2 – 2 ± 0.73 – 72 ± 5 –

–

5.7 ± 0.3

4.44 ± 0.3 1.18 ± 0.6 64 ± 8 8 ± 4 117 ± 9 – From buds Ax. branches 09.09.2000

5.50 ± 0.2 –

– – – – 2 ± 0.28 – 2 ± 0.4 – 4 ± 0.8 – 8 ± 0.61 – 27 ± 7 –

5.72 ± 0.5 –

4.68 ± 0.3 2.18 ± 0.4 37 ± 8 24 ± 4 120 ± 9 – From buds Ax. branches 01.08.2000

6.10 ± 0.2 –

1 ± 0.5 – – – 2 ± 0.27 – 9 ± 0.6 – 2 ± 0.4 – 9 ± 0.68 – 106 ± 11 –

5.47 ± 0.2 –

5.18 ± 0.1 2.15 ± 0.2 13 ± 3 37 ± 10 106 ± 7 – From buds Ax. branches 04.07.2000

5.63 ± 0.1 –

– – – – – – – – 1 ± 0.23 1 ± 0.2 3 ± 0.2 6 ± 0.4 1 ± 0.1 3 ± 0.1 6 ± 0.5 1 ± 0.20 3 ± 0.29 6 ± 0.07 90 ± 5 101 ± 8 93 ± 9

7.02 ± 0.2 6.67 ± 0.2 5.62 ± 0.2

6.98 ± 0.2 6.13 ± 0.3 5.69 ± 0.3 90 ± 8 99 ± 11 101 ± 11 89 ± 6 101 ± 4 93 ± 7 19.04.2000 10.05.2000 04.06.2000

7.03 ± 0.3 6.32 ± 0.3 5.55 ± 0.1

June-cut

No. of attached dead leaves (per shoot)

Uncut July-cut June-cut

No. of live leaves (per shoot)

Uncut July-cut June-cut Uncut

June-cut

Basal stem diameter (mm)

Uncut

Stem density (no. per m−2 )

Nature of regeneration

The morphological characteristics of the two summer-harvested stands compared with that of the control stand are presented in Table 1. In both Juneand July-cut stands, shoot regrowth occurred almost immediately after cutting. The main difference between the two harvested stands in terms of post-cutting regrowth was the nature of their shoot regeneration patterns. In July, 1 month after the June cutting, 74% of the shoots regenerated from the June-cut stand were small axillary branches arising from stubbles left over after harvesting (and 26% arising from rhizome-borne buds). In August, one month after the July cutting, the July-cut stand had regenerated healthy, greener shoots, arising almost exclusively from rhizome-borne buds. By the end of October the percentage of shoots regenerated from buds had increased from 26 to 90% for the June-cut stand, most of the axillary branches having gradually died. However, the July-cut stand did not generate axillary branches at any time after cutting. After shoot harvesting and regeneration, the July-cut stand had wider and longer leaves resulting in higher specific leaf area (data not shown) compared to the June-cut stand (P ≤ 0.05). The stems of the regenerated shoots from both treated stands did not reach the same diameter as those of the uncut stand. The June-cut stand generated shoots with a thinner stem diameter than those of the July-cut stand. Stem diameters of the axillary branches were always less than half of those of the bud-generated shoots. In late October, the regenerated shoot density of June-cut stand, being 110 stems m−2 , exceeded that of uncut stand by 15% while that of July-cut stand being 72 stems m−2 , decreased by 25%. Interestingly, harvesting increased the maximum leaf to shoot dry weight ratios but did not increase the maximum leaf number. Both the June- and July-cut

Table 1 Comparison of the effects of shoot harvesting on the stand structure and morphology characteristics of P. australis

3.1. Shoot regrowth dynamics

July-cut

acteristics, including shoot emergence time, shoot density and height, LAI or above-ground biomass. Similarly, in June, prior to shoot harvesting, ρrhiz (two-way ANOVA; d.f. = 2; F = 0.08; P = n.s.) and total live below-ground biomasses of the uncut and as yet uncut June- and July-cut plots showed no significant differences (P > 0.05) suggesting that the three stands were in similar growth and storage conditions at the time of shoot harvest.

July-cut

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Sampling date

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103

was recorded for the uncut stand (P ≤ 0.05). Maximum of nine leaves occurred in July in uncut stand. After cutting, both stands attained the maximum of ten live leaves by late October. Even though, first sign of leaf death was observed from June, no significant increase was observed until September in the uncut

stands showed leaf to shoot dry weight ratios of about 40% in September, 3 and 2 months after their respective cutting, whereas the maximum ratio attained by the uncut stand was 26% in May. Again in October, June- and July-cut stands showed similar ratios (39 and 37%, respectively), whereas a value of only 10%

Uncut 16

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Biomass (live and dead rhizome and live root) (g m )

0

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Biomass (gm ) (live shoot, stem, leaf and total dead shoot)

250

500

2 Mar Apr May Jun Jul Aug Sep Oct Nov 2000

shoots panicles

stems LAI

0

leaves

Mar Apr May Jun Jul Aug Sep Oct Nov 2000

live rhizome dead rhizome

0

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Fig. 1. Comparison of the seasonal variation of (a–c) above-ground and (d–f) below ground biomass of P. australis in uncut, June-cut, and July-cut stands. Bars and arrows indicate standard error for means and cutting times, respectively.

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stand parts. In late October, both harvested stands had started to show the early signs of shoot senescence. By this time, uncut stand had senesced substantially having only one live leaf and seven attached dead leaves. Fig. 1 illustrates the seasonal variation of above- and below-ground biomass and its components in the Juneand July-cut stands, compared with that of uncut stand. Mean rate of dry matter production (RDP, defined as mean rate of dry matter production per unit ground area between harvests) increased from April to June in uncut stand and until their respective harvesting times in June- and July-cut stands. Over the entire season, the month of June saw the greatest RGR in both the uncut and July-cut stands (0.018 and 0.020 kg m−2 per day, respectively). RDP in uncut stand decreased from July to late October (from 0.004 to −0.012 kg m−2 per day). After June harvesting, RDP remained fairly constant from June through July at 0.001 kg m−2 per day and increased up to 0.005 kg m−2 per day in late October while that of July-cut stand increased from 0.0006 kg m−2 per day in July to 0.006 kg m−2 per day in August and decreased to 0.004 kg m−2 per day in late October. The LAI in late October showed no significant difference (P > 0.05) between the two cutting dates, but a lower LAI for the uncut plots (P < 0.05). However, unlike in the harvested stands, the live shoot biomass in the uncut stand was mostly made up of live stems rather than live leaves, even though all the three stands displayed similar above ground biomass values. Increase of shoot height was relatively slow from early April to mid April but rapid thereafter (Fig. 2). At any time after cutting, neither stands attained the maximum shoot height observed by the uncut stand in August. In late October, the mean shoot height attained by the two harvested stands did not show any significant difference (P > 0.05). No further significant increase in shoot height or shoot biomass was anticipated as both cut stands began forming panicles by October, which coincides with the cessation of the active growth phase of shoots. 3.2. Effects of summer cutting on the seasonal variation of rhizome and root biomass The seasonal pattern in below-ground biomass (Fig. 1d–f) indicates that live rhizome biomass de-

2.5 cut

2.0 Height (m)

104

1.5 1.0 0.50 0.0

Mar

Apr May

Uncut

Jun

Jul

Aug 2000

June-cut

Sep

Oct

Nov

Dec

July-cut

Fig. 2. Comparison of the seasonal variation of shoot height of summer-harvested stands with those of uncut stands. Bars and arrows indicate standard error for means and cutting times, respectively.

creased sharply from April to May, then tended to increase from May to June (P ≤ 0.05). The rhizome biomass values in June were 17–19% higher than the minimum values observed in May after the spring depletion of rhizome reserves. In August, 2 and 1 month after their respective harvesting, the July-cut stand had only slightly but not significantly greater biomass (P > 0.05) than the June-cut stand. Also, the rhizome biomass of these stands was no lower than in June. Given its more vigorous shoot growth than that of the June-cut stand, one would have expected the July-cut stand to have a greater percent reduction in rhizome biomass and reserves in the month following harvesting. But this could not be quantified in terms of rhizome biomass values due to the unavailability of data in July. After August, the rhizome biomass in the June-cut stand remained largely constant while that of the July-cut stand showed signs of mild stand recovery; however the increase was not so significant. In late October when the control stand recorded the highest rhizome biomass (1.96 kg m−2 ), the June-cut stand showed the lowest (1.44 kg m−2 ; P ≤ 0.05) whereas, no significant difference was detected between the June-cut and uncut stands (P > 0.05). Also, dead rhizome and live root biomass did not show a distinguishable seasonal variation pattern during the corresponding period (P > 0.05).

S. Karunaratne et al. / Ecological Engineering 22 (2004) 99–111

105

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600

0.06 0.04 Mar Apr May Jun Jul Aug Sep Oct Nov Mar Apr May Jun Jul Aug Sep Oct Nov 2000 2000 new 1 year

2 years 3 years

4 years 5 years

6 years

Fig. 3. Seasonal variation of age-specific rhizome (a–c) biomass and (d–f) bulk density of P. australis in uncut, June- and July-cut stands. Bars and arrows indicate standard error for means and cutting times, respectively. Standard error for bulk density, omitted for clarity, varied between 0.0006 and 0.0012.

3.3. Effects of summer cutting on seasonal variation of age-specific rhizome biomass and bulk density (ρrhiz ) Seasonal variation of age-specific rhizome biomass and ρrhiz corresponded closely to that of total live rhizome biomass (Fig. 3). Significant post-harvesting differences in age-specific rhizome biomass (three-way ANOVA excluding newly formed rhizomes; d.f. = 5; F = 8782; P < 0.0001), was observed from June to October (three-way ANOVA; d.f. = 2; F = 26.3; P < 0.0001) among the treatments (three-way ANOVA;

d.f. = 2; F = 1018; P < 0.0001). Rhizome biomass (Fig. 3a–c) of 3-, 4- and 5-year-old age categories collectively comprised more than 60% of the total live rhizome biomass at all samplings while 6-year-old rhizome biomass contributed only 1–5% of the total live rhizome biomass. Therefore, the average life span of the P. australis stand in consideration can be estimated as 5–6 years. One to six-year-old rhizome biomass underwent percentage reductions varying from 11 to 53%, similarly in all the three stands from April to May prior to a significant increase from June (P ≤ 0.05). After cutting except for new and 1-year-old rhi-

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zomes, age-specific rhizome biomass did not record a significant increase until the last sampling date in late October in June-cut stand while that of July-cut stand started a gradual increase after August (P ≤ 0.05). However, new and 1-year-old rhizomes in July-cut stand, did not undergo a decrease, but continued to increase steadily until late October even after cutting (P ≤ 0.05). Biomass increment can be considered as an indication of accumulation of storage reserves, increase in structural biomass or a combination of both. However, in all three stands, the ρrhiz of 6-year-old rhizomes, the oldest age category continued to decrease, most probably due to structural death. Though the time of new rhizome formation was delayed until late August or September in the June-cut stand, rather than being in June as it was in the uncut and July-cut stands, new rhizome biomasses at the late October sampling in the harvested stands were not significantly different (P > 0.05). However, the new rhizome biomass of the uncut stand was 47–53% greater than either of the summer-harvested stands. During spring growth in late April, 6-year-old rhizomes had the highest ρrhiz in all the three stand parts, whereas the 1-year-old rhizomes had the lowest (Fig. 3d–f; P ≤ 0.05). Similar to the age-specific rhizome biomass, there was a significant (P ≤ 0.05) reduction in ρrhiz for all age categories from April to May. The ρrhiz of older rhizomes underwent a greater percentage reduction than the younger ones did (P ≤ 0.05). Seasonal minimum ρrhiz for all rhizome age categories occurred between May and June. After spring depletion, ρrhiz was still lowest in young rhizome segments and greatest in older segments. Similar to biomass, significant post-harvesting differences in age-specific ρrhiz (three-way ANOVA excluding newly formed rhizomes; d.f. = 5; F = 36; P < 0.0001), was also observed from June to October (three-way ANOVA; d.f. = 2; F = 26; P < 0.0001) among the treatments (three-way ANOVA; d.f. = 2; F = 23; P < 0.0001). Similar to the spring growth of shoots at the expense of stored reserves in rhizomes, one would expect a decrease in ρrhiz during the shoot regrowth, immediately subsequent to summer cutting. However, no such decrease (P > 0.05) occurred immediately after June harvesting. Except for 2-year-old rhizomes, the first significant reduction in ρrhiz in the June-cut stand occurred between July and August. In contrast, ρrhiz

of all rhizome age categories except 2- and 5-year-old began a significantly decline (P ≤ 0.05) immediately after cutting in July-cut stand. However, overall storage level minima occurred in August for rhizomes of both harvesting treatments. In August, ρrhiz of 3–5-year-old rhizomes was greater (P ≤ 0.05) for the July- than the June-cut stands; however, no significant differences (P > 0.05) were observed for 1-, 2- or 6-year-old rhizomes. From August onwards, ρrhiz began to increase in all age categories, in both harvested stands. Rhizome reserve accumulation rates after the respective seasonal minima for uncut (in May), Juneand July-cut stands (in August) were also calculated. From August through late October, ρrhiz showed a significant increase. For the sake of consistency, the rate of increase in ρrhiz was calculated from May to October for the uncut stand, and from August to October for the June- and July-cut stands. In the uncut stand, the rate of ρrhiz increase from May, after the spring depletion of rhizome reserves, to late October was negatively and linearly correlated (R = −0.87, P ≤ 0.05) with rhizome age (Fig. 4). During the shoot regrowth stage and rhizome accumulation period from August to late October, a similar pattern of negative correlation with rhizome age was also observed for both the June-cut (R = −0.97, P ≤ 0.05) and July-cut (R = −0.98, P ≤ 0.05) stands. Even though both harvested stands had steeper slopes than the uncut stand, the June-cut stand had the steepest slope suggesting a higher accumulation rate, especially in younger rhizome age categories as oppose to a lower accumulation rate in older age categories. This seemed to suggest that irrespective of the type of treatment the younger rhizome age categories accumulated greater amounts of reserves than their older counterparts; however, other factors may also be involved. The greater slope for rate of reserves accumulation (increase in ρrhiz ) of summer-harvested stands also suggests an accumulation capacity stimulated by shoot harvesting, which is greater in younger than older rhizomes. Two-factor ANOVA performed at late October sampling, where new rhizomes were also included, showed highly significant effects of both stand (d.f. = 2; F = 6; P = 0.002) and rhizome age (d.f. = 5; F = 8; P < 0.0001) on ρrhiz . However, the stand factor did not have the same effect at all rhizome ages. Both cutting treatments reduced the storage accumulation ca-

Rate of rhizome bulk density increase (mg mm-3d-1)

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107

0.00070 y = 0.00036067 + -3.5429e-05x R= 0.87

0.00060

y = 0.00072733 + -0.00010829x R= 0.97 y = 0.0005752 + -7.0629e-05x R= 0.98

0.00050 Uncut June-cut July-cut

0.00040 0.00030 0.00020 0.00010 0.0 1 yr

2 yr

3 yrs

4 yrs

5 yrs

6 yrs

Rhizome age

Fig. 4. Age-specific rhizome accumulation characteristics (in terms of rhizome bulk density) of P. australis in uncut (May to late October), June- and July-cut stands (August to late October).

pacity of older rhizome age categories compared to their younger counterparts, the June-cut stand showing the lowest ρrhiz among the stands harvested. However, the ρrhiz of 2-year-old and younger rhizomes did not show a significant difference among the two treatments during late October sampling. Comparison of the ρrhiz of new rhizomes among the three stands at the late October sampling date showed that even though cutting delayed the formation of new rhizomes in the June-cut stand, it has not exerted a significant impact on their reserve storage levels (P ≤ 0.05). In late October, bud characteristics of P. australis were investigated to further elucidate the effects exerted by shoot harvesting on the storage and growth potential of buds formed for the subsequent growing season. The June-cut (4.97 ± 0.26 mm) and July-cut (6.34 ± 0.40 mm) stand gave rise to buds with lesser (P ≤ 0.05) individual diameter than the uncut stand (7.54 ± 0.36 mm). Specific mean bud weight also displayed similar characteristics, having significantly lower (P ≤ 0.05) values in June-cut stands (2.20 ± 0.23 mg mm−1 ), while those of the July-cut stand (3.02 ± 0.26 mg mm−1 ) did not differ significantly from those of the uncut stand ((3.84 ± 0.22 mg mm−1 ). However, no significant difference was observed in the special bud density among the three stands (uncut: 108 ± 24, June-cut: 120 ± 18, July-cut: 102 ± 8 no. per m2 ).

4. Discussion Considering the more or less uniform topography of the selected site, water table, nutrient concentrations of groundwater and the more or less uniform distribution of the shoots in the reed stand, it was assumed that the vigor of shoot growth would be similar in all the three stands and no other external factors, besides cutting, would affect their growth. 4.1. Shoot regrowth dynamics and management implications During the initial stages of post-cutting regrowth, the shoot regeneration pattern, stand structure and above-ground biomass/RDP showed a marked variation between the summer-harvested stands. Rhizomes reached their minimum storage levels in May. Under natural conditions (e.g. uncut stand), a ‘reloading’ of rhizomes from June onwards is indicated by increased rhizome biomass as well as ρrhiz for all rhizome age categories. A similar pattern of total non-structural carbohydrate accumulation in P. australis rhizomes has been observed in Sweden by Graneli et al. (1992), in Switzerland by Haldemann and Brandle (1986) and in Canada by Thompson and Shay (1985). Hence, harvesting P. australis shoots in June halted the process of recharging rhizomes

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from shoot-generated photo assimilates; whereas, by July, rhizomes had accumulated considerable storage reserves. Also, early June saw the lowest number of buds (bud length ≥5 mm) per square meter, for the entire growing season (5–8 buds per m2 ). Haslam (1969) observed a similar phenomenon, in which bud formation virtually ceased temporarily for a few weeks after spring formation of shoots. The June harvesting would have coincided with the rest time of rhizomes during which buds ceased to form. Therefore, it is most probable that in June and immediately thereafter, rhizomes were not ready to form buds and instead axillary branches were generated from the standing stubbles; whereas in July, rhizomes had already begun forming buds, which were subsequently developed into shoots due to the externally applied stress of shoot harvesting. Therefore, if the management strategy is to suppress the growth of P. australis, the best time to remove shoot tissues is when rhizome storage levels are at their lowest or when rhizomes are otherwise resting, which probably occurs in late May to mid June (7–10 weeks after the onset of spring growth) in the Kanto region of Japan where the study site was situated. The specific timing would essentially vary according to the time of spring shoot emergence. Differences in basal stem diameter observed between the two summer-cut stands can be explained on the basis of Haslam’s (1969) observation that within one stand, the size of a bud is determined by the position on the rhizome system from which it arose, and by its season of formation. Therefore, buds formed when rhizomes have lower rhizomes reserves (e.g. June-cut stand) would have smaller diameter, which would subsequently form thinner-stemmed shoots, than buds formed when rhizomes have higher rhizome reserves (e.g. July-cut stand). The larger diameter buds would then form thicker-stemmed shoots. Comparison of stem diameter in August confirms this: July-cut stands produced stems with a 30% greater stem diameter than June-cut stands. The bud formation results further support the above concept. Mean bud (>5 mm in length) diameters measured in August were 6.58 ± 0.38, 4.27 ± 0.31 and 6.17 ± 0.11 mm (mean ± S.E.) in uncut, June- and July-cut stands, respectively. In August, the total live rhizome biomass and mean ρrhiz in uncut, June- and July-cut stands were 2.06 ± 0.11, 1.53 ± 0.06 and

1.66 ± 0.05 kg m−2 and 0.1474 ± 0.0010, 0.1176 ± 0.0009 and 0.1281 ± 0.0004 mg mm−3 , respectively. The above observations also showed that the bud diameter is directly proportional to the rhizome reserve storage, the stand with the highest rhizome storage in August forming the largest diameter of buds, whereas the lowest rhizome storage formed the smallest diameter buds. This was further supported by a corresponding relationship between the bud diameter and the rhizome reserve storage level observed during the late October sampling. Both harvesting treatments increased leaf production, as indicated by their close to two-fold greater leaf/shoot dry weight ratio than in uncut stands. This most probably served to compensate for the loss of assimilatory organs at an important growth phase. The best timing for shoot harvesting for nutrient removal is a major issue in phytoremediation and wastewater treatment facilities using emergent plants such as P. australis. Shoot harvesting at peak shoot biomass is a commonly adopted management practice in many countries. An August harvest (at peak shoot biomass) in Japan is an equivalent to September harvest in many other countries where shoot emergence starts towards the end of April. Present study showed that June harvesting removed 0.69 kg m−2 of shoot biomass, whereas the July harvest removed 1.18 kg m−2 , some 46 and 9% lower, respectively, than the maximum shoot biomass attained by the uncut plots. However, the July harvest removed the seasonal maximum leaf biomass (0.26 kg m−2 ) thereby removing a greater proportion of leaf-bound nutrients than August harvest would have, when the leaf biomass was only 0.22 kg m−2 (uncut stand). Karunaratne and Asaeda (2002) showed that P. australis contains an average of 2.2, 1.9, 1.7% shoot-bound nitrogen and 0.22, 0.19, 0.16% shoot-bound phosphorous in early June, July and August (at peak shoot biomass), respectively. Therefore, June and July harvesting removed 144, 228 kg ha−1 shoot-bound nitrogen and 14, 23 kg ha−1 shoot-bound phosphorous, respectively. This estimation showed that July harvesting almost doubled the removal of shoot-bound nutrients. An August harvest would remove 219 and 20 kg ha−1 of shoot-bound nitrogen and phosphorous, respectively. Considered the fact that the leaf tissues have a higher nutrient content than stem tissues, the above estimate is a lower limit for the shoot-bound nutrients. There-

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fore, July harvesting, which removes the maximum leaf biomass, may also remove a greater quantity of nutrients than an August harvest, even if the total shoot biomass removed is slightly lower. Since significant leaf senescence and abscission occurred from August onwards, and remaining leaves became tougher, they would be increasingly poor in nutrients and palatability as the end of the growing season approached. Therefore, if the harvested shoots are to be used for forage, July (a higher leaf biomass) or early (lower leaf biomass) harvesting may make them more palatable. Further, the observations at the same site during the subsequent 2001 growing season showed that the June-cutting had been more effective in reducing next year’s shoot growth than had the July-cutting (Asaeda et al., unpublished data). Such an outcome has also been indicated by George (1992), Gryseels (1989), Weisner and Granely (1989) and Husak (1978). In 2001, maximum shoot biomass in the June 2000-cut stand was 27% less than that of the uncut, whereas no such difference was apparent between July 2000-cut and uncut stands. Though shoot density was slightly higher in the previous-June-cut stand than in the previous-July-cut stand, stand vigour and fitness (assessed in terms of stem diameter, specific leaf area, condition of panicle formation, shoot biomass and shoot height) were poorer in the previous June-cut stand, whereas the previous July-cut stand performed in a manner similar to the uncut stand portions. Hence, it can be seen that this study has major implications for the management of reed swamp communities: harvesting in June suppresses the growth of the reed, especially in the following year(s), while harvesting in July or August, if the stand is used in treating wastewater maximizes nutrient removal while preserving a healthy stand for subsequent years. Further, repeated June-cutting may likely weaken the stand beyond repair after several years. 4.2. Seasonal variation of age-specific rhizome storage dynamics Karunaratne et al. (in press-ab) proposed that older rhizomes support the spring formation of shoots more so than the younger rhizomes. Accordingly it would be quite reasonable to assume that after harvesting

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of shoots, the rhizome reserves should decrease due to formation of new shoots similar to the spring remobilisation of rhizome reserves. Immediately after harvesting the shoots in July (July-cut stand), the rhizome reserves were depleted due to formation of new shoots, which used stored rhizome reserves. However, this was not the case after the June harvesting, as no significant depletion of rhizomes reserves occurred, ρrhiz remaining more or less constant until July and starting to decrease only afterwards. Also the same observations were made during a preliminary study at a nearby P. australis stand in 1999. It is most probable that the axillary branches formed in the June-cut stand after mowing did not draw as much stored resources from the rhizomes as did those of the July-cut stand. Also a portion of the photo assimilates produced by these shoots might have been translocated to the rhizomes from the early stages (after shoot harvesting) to form new buds. This assumption was supported by the early death of most of the axillary branches from August onwards, which could also be partly due to the shoot senescence. The new rhizome characteristics observed in this study implies that even though the summer harvesting may limit the clonal expansion to some extent, the timing of harvest might not be significant. However, the present data are insufficient to strongly support the above proposal because of the possibility of underestimating the below-ground biomass values in the late October sampling due to continuously high water levels at the study site after heavy seasonal rains. The rhizome and root biomass measurements during this sampling showed comparatively lower values than expected. The reduction in mean ρrhiz of rhizomes after the summer harvesting (during the shoot regeneration from June/July to August) were only 7.0 and 6.6% for June- and July-cut stands, respectively, whereas the reduction in the mean ρrhiz during spring shoot formation was over 23%. However, the remaining resource storage level at the end of spring depletion of rhizomes would suggest that the rhizomes still contained sufficient carbohydrates to fuel growth of approximately three growing seasons without any recharging. According to Graneli (1992) P. australis maintains large, under-utilised stores of resources to enhance the fitness of the stand, by ensuring establishment of spring shoots in a stochastic environment that period-

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ically reduces rhizome standing stocks of resources or increases demand for resources. Accordingly, unusually high rhizome mortality in winter or loss of spring shoots due to frost could threaten clone competitiveness and survival if adequate reserves were not available for spring shoot establishment or reestablishment. However, the reduction of mean ρrhiz after the summer treatments suggests that Graneli’s (1992) proposal would only hold during the initial growth phase of a P. australis stand, i.e. during the period of spring formation of shoots. Even though the rhizomes still contained sufficient stored reserves after the summer cutting to theoretically form an equally vigorous above ground stand similar to the uncut stand, this did not occur. It appears that the growth performance of the stand after summer harvesting was driven by a biological time clock, dependant also upon temperature, rather than solely on the level of rhizome reserves.

5. Conclusions The study identified the quality of the seasonal changes of the rhizome reserves as essential for proper vegetation management. Significant differences in the post-harvest shoot regeneration pattern, morphology and rhizome storage and resource translocation dynamics showed that selection of shoot harvesting time should essentially be based on the desired management goal. As the post-harvesting shoot and rhizome dynamics differ strongly depending on the rhizome storage level at the time of shoot harvesting, even in the same stand where shoots are harvested yearly, cutting time should be determined considering the spring shoot formation time.

Acknowledgements The authors thank the Akigase Park office, Saitama, Japan for kindly allowing them to carry out the fieldwork within the Park premises. The authors are also thankful to W. Sasaki, Ira and Prathima for their help in the fieldwork and the laboratory analyses. Authors would also like to thank F. Salehi and his colleagues at McGill University, Canada for the linguistic help and valuable comments.

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