Research Article |
Corresponding author: François-Marie Martin ( francois.martin@irstea.fr ) Academic editor: Ruth Hufbauer
© 2020 François-Marie Martin, Fanny Dommanget, François Lavallée, André Evette.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Martin F-M, Dommanget F, Lavallée F, Evette A (2020) Clonal growth strategies of Reynoutria japonica in response to light, shade, and mowing, and perspectives for management. NeoBiota 56: 89-110. https://doi.org/10.3897/neobiota.56.47511
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Many of the most invasive plant species in the world can propagate clonally, suggesting clonality offers advantages that facilitate invasion. Gaining insights into the clonal growth dynamics of invasive plants should thus improve understanding of the mechanisms of their dominance, resilience and expansion. Belonging to the shortlist of the most problematic terrestrial invaders, Reynoutria japonica var. japonica Houtt. (Japanese knotweed) has colonized all five continents, likely facilitated by its impressive ability to propagate vegetatively. However, its clonal growth patterns are surprisingly understudied; we still do not know how individuals respond to key environmental conditions, including light availability and disturbance. To contribute to filling this knowledge gap, we designed a mesocosm experiment to observe the morphological variation in R. japonica growth in homogeneous or heterogeneous conditions of light stress (shade) and disturbance (mowing). Rhizome fragments were planted in the middle of large pots between two habitat patches that consisted of either one or a combination of the following three environmental conditions: full light without mowing, full light with frequent mowing, or shade without mowing. At the end of the experiment, biomass and traits related to clonal growth (spacer and rhizome lengths, number of rhizome branches, and number of ramets) were measured. After 14 months, all individuals had survived, even those frequently mowed or growing under heavy shade. We showed that R. japonica adopts a ‘phalanx’ growth form when growing in full light and a ‘guerrilla’ form when entirely shaded. The former is characteristic of a space-occupancy strategy while the latter is more associated with a foraging strategy. In heterogeneous conditions, we also showed that clones seemed to invest preferentially more in favorable habitat patches rather than in unfavorable ones (mowed or shaded), possibly exhibiting an escape strategy. These observations could improve the management of this species, specifically by illustrating how aggressive early control measures must be, by highlighting the importance of repeated mowing of entire stands, as this plant appears to compensate readily to partial mowing, and by informing on its potential responses towards the restoration of a cover of competitive native plants.
clonal growth, environmental heterogeneity, Fallopia japonica (Polygonum cuspidatum, Japanese knotweed), invasion dynamics, lateral expansion of patches/stands, spatial spread, vegetative regeneration
Clonality is an attribute frequently associated with plant invasiveness (
At the local scale, since performance and impact of invasive clonal plants are often directly related to their clonal growth characteristics (e.g. architectural traits, lateral growth rate, ramet density, clonal integration, growth strategies), understanding clonal growth patterns and strategies is of prime importance for improving management strategies. This is why the clonal growth dynamics of many highly problematic clonal invaders have been the subject of extensive research over the years: e.g. Phragmites australis (
Despite being listed as one of the worst invasive plants in the world (
Two important features of environments that correspond to two main means of managing R. japonica are light availability and disturbance. Reynoutria japonica is mainly found in high-light habitats, but closed-canopy habitats such as forests can still be colonized either directly from vegetative propagules, or from the lateral expansion of surrounding populations (
To improve our understanding of R. japonica’s invasion dynamics, specifically how clonal growth responds to important environmental factors, we designed a mesocosm experiment. In it, we explore how the development and expansion of young clonal fragments is affected by homogeneous or heterogeneous conditions of light stress (shade) and disturbance (mowing). We aimed to better understand plant growth strategies and potential trade-offs when faced with more or less favorable habitats, and investigate how these responses might be relevant to improved management of R. japonica by mowing/cutting or by ecological restoration using dense cover of competitive species. We hypothesized that: i) a homogeneously high light availability would favor aggregation of ramets while a homogeneous shade would favor a more scattered distribution of aerial shoots, two growth forms respectively known as phalanx and guerrilla (sensu
In April 2017, rhizomes belonging to a single R. japonica individual were manually excavated. The plant was located outside the village of Cholonge (1061 m a.s.l.; 45°00'N, 5°79'E), in the French Alps. This individual was chosen because it was growing in an open and unmanaged site. This was an important prerequisite since we wanted to limit the chance that ramets growing from its rhizome fragments were influenced by stressful or disturbed conditions via transgenerational inheritance (
Following excavation, rhizomes were washed and cut to obtain homogenized fragments with the same approximate weight and number of nodes. The thirty most similar fragments were selected, bagged and stored in a cold room before the start of the experiment. These fragments had a mean weight of 16.44 g (± 0.85 g) and a mean number of nodes of 8.06 (± 2.46).
The mesocosm experiment was conducted in an experimental nursery of the National Forest Office (ONF) located in Guéméné-Penfao, Brittany (France). The area is characterized by mean monthly temperatures ranging from 7.9 to 16.4°C, and 694 mm of mean annual precipitation (data from Rennes meteorological station; www.meteofrance.com).
The experimental design was composed of five treatments with six replicates each. The treatments were designed to enable us to evaluate how R. japonica responds to homogeneous or heterogeneous environmental stressors. Each plant was grown in pots divided into two habitat patches. These habitat patches were identical for homogeneous treatments: light without mowing (L), light with mowing (M), and shade without mowing (S). For heterogeneous treatments, they differed: half-light – half-mowing (LM) and half-light – half-shade (LS); Fig.
Experimental design. The different colors represent the treatments: green (un-shaded and un-mowed habitat), pink (un-shaded but mowed habitat) and grey (shaded but un-mowed habitat). Each of these five different treatments had six replicates. The red segments in the middle of “pots” represent the position of the rhizome fragments that were planted
Large pots for this experiment were created from thirty rainwater tanks of ca. 1000L (120 × 100 × 116 cm) by cutting off their tops. Pots were first filled with a 15 cm layer of gravels (Ø 0–32 mm) to facilitate water drainage through an outlet pipe. On top of that, we added approximately 100 cm layer of a certified substrate composed of 70% river sand, 15% loam and 15% compost (chemical composition of the substrate: N = 1.2%; K2O = 1.4%; P2O5 = 0.4%; MgO = 0.6%; CaO = 2.1%: C:N = 12; pH = 8–9). Shade treatments (S and LS) were created by inserting 3 m poles into the pots and covering them with netting that filtered around 80% of the light. Pots were arranged in a flat area, with their location and orientation randomly chosen in such a way that each replicate of a given treatment had a different orientation from the other five replicates. To avoid the effect of projected shadows caused by the tall shade treatments, pots were separated by 4 m intervals in every direction. Additionally, the randomized placement and orientation of all the pots was reshuffled in the middle of the experiment.
In early May 2017, the thirty rhizome fragments were randomly assigned to one of the pots. They were buried two centimeters below the surface in the middle of the pots, orthogonally to the greater length of the pots. This position coincided with the limit between the two habitat patches of the pots (Fig.
Before each mowing event, the number of ramets in each habitat patch was recorded. We decided to stop the experiment when ramets began to reach pots’ edges, to minimize obstacle-effects on the clonal architecture of the plants (duration of the experiment = 420 days; ca. 14 months).
The experiment was harvested at the end of June 2018. All ramets growing aboveground in all habitat patches were counted before being clipped and oven-dried for 48h at 100 °C prior to measuring dry biomass. Additionally, the horizontal distance between the farthest ramet and the center of the pot (i.e. the location of the rhizome fragment initially planted) was measured for each half of each pot to estimate maximal lateral expansion distances for developing stands. We then carefully excavated the plants, using mostly our hands and screwdrivers in order not to break fragile rhizomes and buds, and to extract rhizomatous systems as intact as possible. However, roots were intentionally cut to facilitate excavation, as our hypotheses were unrelated to the root system. We then marked the position of the separation line between the two habitat patches on each rhizomatous system before removing the dirt with an air compressor and brushes. Rhizome and spacer lengths (see below), number of rhizome branches, and number of axillary and basal buds that were growing in each habitat patch were measured. Finally, we also measured rhizome biomass with the same method as for aboveground tissue.
We follow
Prior to analyses, data were explored and prepared following the protocol of
Since R. japonica’s clonal growth patterns and processes are largely unknown, the first steps of our analyses were necessarily exploratory and descriptive. To investigate our hypotheses however, the responses of variables characterizing R. japonica’s growth form and strategies were analyzed more thoroughly. These variables were biomass (aboveground, rhizomatous and total dry biomasses in grams), specific spacer length (length of a spacer per unit of biomass), number of ramets (accounted for as the number of aerial shoots) and rhizomes’ branching frequency (calculated as the number of rhizome branches per unit of rhizome length). Analyses were performed at two different scales: (i) pots and (ii) half-pots. As a reminder, in our experimental design there were two habitat patches per pot, identical or not, but only one plant (Fig.
(i) At the pot scale, measurements made within the two habitat patches of each pot were summed up so as to have observations at the individual level. As such, whole plants were taken as statistical units and our five treatments (L, M, S, LM, and LS) were used as explanatory factors. For each response variable, we performed ANCOVAs with type II Sums of Squares and used the weight and number of nodes of initially planted rhizomes as covariates. For multiple comparisons, we used pairwise t-tests using Holm-Bonferroni corrections to control for family-wise error rates.
(ii) At the half-pot scale, observations were made at the sub-individual level (i.e. half plants) and differences linked to differing growing conditions between habitat patches were investigated, but only for replicates belonging to heterogeneous treatments (LM and LS). As the two half-plants of each pot were not independent, we used mixed-ANCOVAs with pot as a random effect (
Initially, we also wanted to study potential differences in the number of buds between treatments as evidence of habitat selection, but we observed during harvest that R. japonica produces a bud at each node regardless of the treatment, precluding further analysis.
All analyses were performed with R version 3.5.2 (
Consistent with what is reported in the literature (
All rhizomes that were planted at the beginning of the experiment gave birth to clonal fragments that survived throughout the 14 months of the experimentation. Interestingly, most clones produced flowers in the first growing season except those of the entirely mowed treatment (M).
As expected, most traits related to clonal growth varied strongly by treatment (Tables
Summary statistics of descriptive variables measured across all treatments (at the pot scale).
Maximum spacer length (cm) | Mean spacer length (cm) | Cumulated rhizome length (cm) | Mean rhizome length (cm) | Longest length between opposite ramets (cm) | Number of rhizome branches | Number of buds (on rhizomes) | Number of ramets (aerial shoots) | Aboveground dry biomass (g) | Rhizomatous dry biomass (g) | Total dry biomass (g) | |
---|---|---|---|---|---|---|---|---|---|---|---|
Mean | 56,07 | 30,59 | 599,2 | 16,65 | 68,98 | 24,6 | 230,42 | 23,97 | 499,45 | 207,04 | 706,49 |
Standard deviation | 29,22 | 24,55 | 519,03 | 6,94 | 39,43 | 24,4 | 159,3 | 13,25 | 404,48 | 200,8 | 591,5 |
Median | 53,25 | 23,27 | 484,7 | 16,32 | 68 | 17,5 | 220,5 | 22,5 | 325,5 | 98,38 | 394,52 |
Minimum | 17,1 | 1 | 38,9 | 3,367 | 6,5 | 1 | 19 | 5 | 1,21 | 9,01 | 10,22 |
Maximum | 112 | 92,5 | 2113 | 29,18 | 133 | 97 | 638,92 | 55 | 1221 | 708,66 | 1902,66 |
Clones in the L treatment (full light without mowing) produced their farthest ramets (from their center) farther than individuals of any other treatments and with a far lower variability (Table
Descriptive statistics by treatment for the distance to the farthest ramet in each habitat patch (pot-half).
L | M | S | LM | LS | |
---|---|---|---|---|---|
Mean | 56,17 | 11,63 | 34,50 | 53,83 | 36,58 |
Standard deviation | 6,70 | 7,06 | 23,85 | 19,31 | 23,46 |
Median | 56 | 11,5 | 38 | 57,5 | 34 |
Minimum | 45 | 1,5 | 5 | 15 | 5 |
Maximum | 66 | 25 | 70 | 75 | 66 |
In all our analyses, covariates did not significantly influence examined responses. Consequently, observed differences could be attributed to treatments. Unsurprisingly, shade and mowing treatments significantly reduced total biomass production (F = 89.36; dfn = 4, dfd = 26; p < 0.001), aboveground biomass production (F = 43.18; dfn = 4, dfd = 26; p < 0.001) and rhizomatous biomass production (F = 57.03; dfn = 4, dfd = 26; p < 0.001; Fig.
Differences in total dry biomass (a), aboveground biomass (b) and rhizomatous biomass (c) between the L (light), M (mowed), S (shaded), LM (half-light – half-mowed) and LS (half-light – half-shaded) treatments. For analyses at the pot scale, letters are used to indicate the significance level of differences (treatments not sharing the same letter were significantly different at p < 0.05). For analyses at the half-pot scale, stars are used to indicate significant differences between habitat patches (* = p < 0.05; ** = p < 0.01; *** = p < 0.001; ns = not significant). As a reminder, differences among pot-halves have only been investigated for heterogeneous treatments (i.e. LM and LS).
At the scale of pots, individuals of R. japonica growing in full light without mowing (L) had significantly lower specific spacer lengths than clones growing in fully shaded habitats (S; t = 4.361, p < 0.001) and entirely mowed individuals (M; t = 3.005, p < 0.025). At the half-pot scale, despite a slight trend of increased specific spacer length for spacers growing in the shaded habitat patches of the LS treatment, no significant differences were found within or among heterogeneous treatments (Fig.
Differences in specific spacer length between L (light), M (mowed), S (shaded), LM (half-light – half-mowed) and LS (half-light – half-shaded) treatments at the scale of pots (a) or half-pots/habitat patches (b). Treatments not sharing the same letter are significantly different at p < 0.05, ns = not significant.
Shading (S) led to the production of fewer ramets than full light (L) (t = -7.327, p < 0.001) and mowing (M) (t = -8.23, p < 0.001), and there was no differences between full light and mowing in number of ramets (t = 0.276, p = 0.89; Fig.
Differences in number of ramets between L (light), M (mowed), S (shaded), LM (half-light – half-mowed) and LS (half-light – half-shaded) treatments at the scale of pots (a) or half-pots/habitat patches (b). For the former, treatments not sharing the same letter were significantly different at p < 0.05, while for the latter: * = p < 0.05; ** = p < 0.01; *** = p < 0.001; ns = not significant.
Finally, clones in pots receiving full light (L) had a significantly higher rhizome branching frequency than shaded clones (S) (t = -2.686, p = 0.032), but not higher than entirely mowed clones (M; t = 0.393, p = 0.267) while LM and LS clones showed intermediate values (Fig.
Differences in rhizome branching frequency (measured as the number of branches per unit of rhizome length) between L (light), M (mowed), S (shaded), LM (half-light – half-mowed) and LS (half-light – half-shaded) treatments at the scale of pots (a) or half-pots/habitat patches (b). For the former, treatments not sharing the same letter were significantly different at p < 0.05, while for the latter: ns = not significant.
Despite its importance for understanding and managing local invasion dynamics of R. japonica and its congeners, the clonal growth of this taxon and its variations under various environmental conditions have been surprisingly understudied (
Our results show that R. japonica can respond plastically to the quality of its habitat in various vegetative growth traits. In accordance with our first hypothesis, R. japonica adopted a phalanx growth form when growing in a homogeneously illuminated habitat by aggregating many ramets separated by short spacers. Conversely, when growing under heavy shade, clones only presented a few ramets separated by long spacers, typical of a guerrilla growth form (Figs
Although clones growing in full light without mowing expanded laterally more than shaded ones in absolute values (Tables
In theory, phalanx individuals should have a slower lateral expansion rate than guerrilla individuals (
Against our expectations, average ramet densities and branching frequencies of entirely mowed clones in full light (M treatment) were not significantly higher than those of illuminated but un-mowed ones (L treatment), despite interesting trends. Moreover, entirely mowed individuals had an overall very low spatial expansion. This discrepancy between our hypothesis and observations is likely due to the intensity of mowing events. As these clones had to cope three times with the total destruction of their aerial organs during their first growing season (and one more time at the beginning of the next one), their biomass production and spatial exploration must have been strongly constrained (Fig.
Stands of R. japonica frequently grow in habitats that do not experience full sun, or are mowed, such as roadsides, semi-natural riverbanks or forest edges (
The absence of clearer morphological and architectural responses in the heterogeneous treatments may be simply linked to the methodological constraints related to the cultivation of giant herbaceous species such as R. japonica: i.e. small sample size and short duration of experimentation. A longer experiment, with a harvest at the end of the second growing season could perhaps have given different results, for instance for the significance of observed differences or bud bank’s distribution (cf.
In addition to increased sample size, it would be interesting if future experiments could increase the number of sampled populations. Reynoutria japonica is indeed known to be represented by the same single clone throughout most of its introduced range (
Although this experiment did not aim at investigating the establishment potential of R. japonica, it is enlightening to observe that the thirty regenerating plants survived their first winter and were still growing after 14 months. It is even more interesting when we consider that some had to grow under heavy shade or in a frequently mowed environment. It confirms that three mowing events per year is not sufficient to kill regenerating clones of R. japonica (
The vegetative propagules that we planted had a fresh weight of approximately 16 g, which represents rhizomes with a length of 12–13 cm for a diameter of 1.2 cm. Such dimensions are certainly not infrequent in the wild where R. japonica can annually produce underground biomass exceeding 10 t · ha-1 (
Interestingly, clones that experienced only partial mowing (LM treatment) did not produce a significantly lower total biomass than un-mowed individuals (L treatment). Yet, the contrast with the biomass production of entirely mowed clones (M treatment) is striking (Fig.
Restoration of competitive native species has been shown to be a promising management solution to limit the performances and spread of R. japonica (
To the best of our knowledge, this is the first time that quantitative observations of clonal growth and expansion dynamics in R. japonica are provided for differing environmental conditions. We believe that our results help improve our understanding of the invasion dynamics of this species at the local scale, highlighting aspects of its resilience and effects on invaded communities that will be useful for the management and modelling of this taxon. However, more research is needed to complete our results and to extend them to other knotweed taxa as well as to other epigenotypes of R. japonica.
We are deeply grateful towards Olivier Forestier, Philippe Poupart and Emeline Rousset for their help in the preparation and data collection of this study. We also thank Cendrine Mony, Jake Alexander, Ruth Hufbauer and an anonymous reviewer for their helpful comments on the manuscript. Finally, we are grateful towards the ITTECOP-Dynarp project and the ONF (Office National des Forêts) for their technical and financial support.