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Quantifying macrophyte colonisation strategies—A field experiment in a shallow lake (Lake Balaton, Hungary)
Aquatic Botany 136 (2017) 56–60
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Quantifying macrophyte colonisation strategies—A field experiment in a shallow lake (Lake Balaton, Hungary) Ágnes Vári ∗ , Viktor R. Tóth Balaton Limnological Institute, Centre for Ecological Research, Hungarian Academy of Sciences, 8237 Tihany, Klebelsberg K. u. 3, Hungary
a r t i c l e
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Article history: Received 11 October 2013 Received in revised form 12 September 2016 Accepted 15 September 2016 Available online 16 September 2016 Keywords: Regeneration Fragment rooting Rhizomatic growth Life-history Phenology Biomanipulation Lake recovery
a b s t r a c t Life-history traits like dominance of certain reproductive modes (e.g. vegetative, specialized, unspecialized or sexual propagules) and overwintering strategies (evergreen or re-sprouting) determine the success and timing of the ability of aquatic plants to colonize new areas. In the present experiment the distribution of these reproductive modes was examined in-situ, where new gaps were experimentally formed and establishment of new vegetation observed on a monthly bases in ten plots. During a period of 126 days, altogether 73% of all established plants (n = 1822) colonized by rhizomatic growth and 11% by rooting of vegetative fragments. Myriophyllum spicatum was observed to use mostly fragment rooting (81%), while Potamogeton perfoliatus followed a more mixed strategy combining re-rooting fragments and rhizomatic growth (31% and 41%, respectively). Stuckenia pectinata also preferred colonisation by rhizomes (84%). No colonisation by specialized vegetative units (tubers or turions) was observed during the study period The importance of surrounding vegetation was shown by comparing colonisation on inner and marginal sections of the plots (30% vs.70%). Three different patterns of timing of peak colonisation intensities were observed, related to species’ life-history traits. While several experimental works have been done on the regeneration and colonisation abilities of different species under laboratory conditions, information on the in-situ application of the different strategies is scarce. Insights on the modes by which plants succeed in colonising gaps helps us understand how (re)establishment of aquatic vegetation might function in lake ecosystems recovering after eutrophication. © 2016 Elsevier B.V. All rights reserved.
1. Introduction Plants, thus submerged aquatic macrophytes too, can propagate by both vegetative and sexual means. Macrophytes usually use a wider range of possible modes for establishing in new areas and in newly emerging patches than terrestrial plants do, thereby being able to colonize a diversity of habitats (Barrat-Segretain, 1996; Sculthorpe, 1967). This multiplicity of colonisation modes makes it possible to investigate the relationship between life-history traits (like different ways of reproduction) and colonisation success. Re-colonisation can occur on different spatial scales: locally, following either minor disturbance (such as strong currents or waves, which can dislocate bundles of plants, or feeding, trampling, boat movements), or major disturbance events, which eradicate
∗ Corresponding author. Present adress: Institute of Ecology and Botany, Centre for Ecological Research, Hungarian Academy of Sciences, 2163 Vácrátót, Alkotmány u. 2-4, Hungary. E-mail address: [email protected] (Á. Vári). http://dx.doi.org/10.1016/j.aquabot.2016.09.006 0304-3770/© 2016 Elsevier B.V. All rights reserved.
greater areas of aquatic vegetation (such as ice-scouring, drought or floods (Barrat-Segretain and Amoros, 1996; Kautsky, 1988), or at the whole lake-level, when a lake returns (through reoligotrophication) from algae-dominated turbid state that resulted from previous eutrophication (Scheffer, 1990; Scheffer and Van Nes, 2007). Re-establishment of macrophytic vegetation after return from high eutrophication levels is a common issue, especially in shallow lakes world-wide (excellent review by Bakker et al., 2012; Galanti et al., 1990; Hilt et al., 2010; Hobbs et al., 2012; Jeppesen et al., 2005; Lauridsen et al., 2003, 1994; Ozimek, 2006), as it is also in the study area Lake Balaton (Herodek et al., 1988; Istvánovics et al., 2007). This article argues that looking into details at the small scale might elucidate the potentials and limitations of processes on the large scale, whole-lake level. Colonisation by plants can be regarded as conquering new areas, establishing from propagules which arrived from other areas to that patch. Regeneration is seen as the process by which plants re-grow from some part of the whole plant, which might be below-ground or not (e.g. Barrat-Segretain et al., 1998; Umetsu et al., 2012). For the purpose of this study we defined (similarly to Capers, 2003
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and to Henry et al., 1996) all mechanisms of establishing new, aboveground canopy as colonisation, as they are all ways by which previously non-visible plants appear in the standing vegetation and can participate in further life-history events. Life history is composed of survival probabilities and rates of reproduction (Partridge and Harvey, 1988), including patterns of development, growth, reproduction and lifespan (Fabian and Flatt, 2012). The development of both vegetative and generative reproductive structures is determined by different life history traits and phenology, which in turn act on potential speed and timing of colonisation. Within the diversity of reproductive options open to a macrophyte, there are two major ways of reproduction, depending on whether a species overwinters solely as sexual propagules (as annuals do) or in some vegetative shape (like perennials). Overwintering in perennials can take place by receeding to underground plant parts, while some aquatic perennials remain partly green above-ground. The latter start in spring with a head start in developing biomass. Colonisation of newly available areas depends, apart from patch suitability, also on the surrounding vegetation within the waterbody, the effect of which is mostly detectable at the boundaries of gaps (e.g. Capers, 2003; Henry et al., 1996). Testing the effect of gap edges throws light on the importance of already existant macrophytic vegetation as kernels of (re)establishment. The set of reproductive options a species can resort to is delimited and timed by its life-history, whereas the relative importance with which the different colonisation modes are used also depends on the local environment (Capers, 2003; Wiegleb and Brux, 1991). However, it is expected that there are species-specific propagation strategies combining the available options in a characteristic way, but in lake ecosystems this has never before been quantified in-situ. Differences in the preference of colonisation modes might explain spatial as well as temporal patterns of macrophyte occurrence. Therefore, we wanted to investigate, a) whether different macrophyte species use different strategies in colonising and to quantify the propagation modes in relation to each other. In order to test the source of colonisation, we hypothesized that b) edge-effects would be strong, and c) there would be differences between the months in summer and autumn in colonisation intensities, relatable to the species life history traits.
2. Material and methods Ten plots of 1 m × 1 m were randomly designated in 0.6–1.0 m deep water in Lake Balaton (coordinates: 46◦ 54 50.26 N 17◦ 53 36.38 ) on 4th June 2009. Plots were arranged on four points (sub-sites), within a range of 5–70 m apart. The site represented the typical submerged vegetation of Lake Balaton with Potamogeton perfoliatus L., Stuckenia pectinata (L.) Böerner, Myriophyllum spicatum L., Ceratophyllum demersum L. and Najas marina L., belonging to the category of “Euhydrophyte vegetation of naturally eutrophic and mesotrophic still waters” in the national vegetation catalogue (Bölöni et al., 2011). At the start of the experiment, all vegetation was removed from the plots by hand, equipped with scuba diving gear, while care was taken to remove attached subterranean parts of the existent plants as completely as possible. We did not sift through the sediment in order to remove detached propagules, following the approach of Capers (2003). Plots, divided into a margin (outer 15 cm within the plot) and an inner section, were treated every 3–4 weeks (on 07/07, 03/08, 10/09 and 08/10) until the end of the vegetation period. Each time, all newly grown vegetation was carefully removed while checking whether it had established by one of the following colonisation modes suggested by Capers (2003) and own observations:
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1 by re-rooting of vegetative fragments (detectable by the blackened, slightly decomposing endings of a (half-buried) shoot) 2 by clonal (rhizomatic, lateral) growth from neighbouring plants (physical attachment to plants through their rhizomes outside the plot) 3 by re-sprouting of specialized vegetative propagules (turions or tubers) (recognizable by the remnants of the vegetative propagule that sprouted) Germination of seeds was not included in the assessment of the different colonisation modes as this probably mostly occurs during spring-time, which was not covered by the present study. If the colonisation event did not fall into any of the above categories, it was noted as “unknown”. C. demersum and N. marina fragments were often found on the plots without rooting, but as fragmentation and being unrooted belongs to their normal lifecycle, these events were counted as colonisation by fragments. In order to calculate colonisation potentials for the different species, plants were counted and species determined. In compliance with our definition of colonisation, each plant, possibly with several shoots or ramets that appeared on the treated plots was regarded as one colonisation event. This means that for C. demersum, which roots only with some minor rhizoids or not at all, colonisation was counted as such if any shoots were found lying on the sediment surface. The same applied for N. marina, which is also often found towards the end of the summer unrooted, seemingly without losing vitality. In order to take into account the correlated observations, generalized estimating equations (GEE) were applied with an assumed Poisson-distribution, implemented in SAS SAS University Edition, Version 2.2 (SAS/STAT). In order to control for potentially confounding effects, the GEE model included apart from species, plot-section (inner and outer) and date of sampling, also time since last vegetation removal (in days), interaction between species and plot-section as fixed effects and sampling site (A, B, C and D), as random effect. First order auto regressive covariance structure was used to describe the within plot error distribution. Fixed effects were tested at alpha level of 0.05 by means of Wald-test. Least squares mean estimations of abundancies in inner and outer plot sections and their geometric means ratios (GMRs, inner/outer) with corresponding Tukey – type 95% confidence intervals were derived. Differences between species in the distribution of colonisation modes were tested with G-test of independence in R version 3.2.2 for all months and for separate month too, in order to check results independently from date (R Developement Core Team, 2016). 3. Results A total of 1822 plants established during the whole research period from 7th June till 8th October (126 days), resulting in an overall colonisation rate of 1.4 plants per day per m2 . Most intense colonisation took place during August (peak value from harvesting on 7th September) with 85.1 ± 15.7 colonisation events per m2 on average (± SE), while it was lowest during the following month, harvested at the beginning of October (19.8 events ± 2.8). First it was M. spicatum and C. demersum which colonized most actively, during June (resulting in peak value sampled on 7th July), both declining steadily throughout the study period, with M. spicatum slightly increasing again in October (Fig. 1, Table 1). N. marina colonisation rates peaked next, in early August. In S. pectinata and P. perfoliatus most plants established during August, giving a maximum at the sampling on 10th September, exceeding plant densities of M. spicatum. Almost three quarters of all noted colonisation events (73%) could be assigned to rhizomatic growth from surrounding plants,
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Á. Vári, V.R. Tóth / Aquatic Botany 136 (2017) 56–60 Table 3 Colonisation modes used by the newly established species in the cleared plots in%. “rhizome” – rhizomatic growth, “fragment” – fragment rooting, “unknown” – could not be determined with certainty or was none of the hypothesized categories.
Ceratophyllum demersum Myriophyllum spicatum Najas marina Stuckenia pectinata Potamogeton perfoliatus total
Fig. 1. Colonisation events (plants per m2 ) for the species observed colonising experimentally de-vegetated plots during the study period in summer and autumn. Plants were summed up for each species and divided by 10 (=total area of clearance; number of plots) to get the mean plant densities/m2 . Note the second axis used for showing S. pectinata densities.
Table 1 Colonisation events (plant densities per m2 ± SE) in whole plots for each colonising species and date. Counted plants are summarized per species and date and divided by total area. species
Ceratophyllum demersum Myriophyllum spicatum Najas marina Potamogeton perfoliatus Stuckenia pectinata
date 07/07
03/08
10/09
08/10
0.7 7.4 ± 2.3 0.2 1.6 ± 0.6 28.7 ± 20.9
0.2 ± 2.5 3.7 ± 1.0 3.6 ± 4.5 2.3 ± 1.1 29.1 ± 18.1
0.2 2.0 ± 0.6 0.6 2.4 ± 5.5 79.9 ± 95.5
0 2.4 ± 1.6 0.4 ± 1.0 2.0 ± 1.2 15.0 ± 4.3
Table 2 Summary of GEE model fixed effects analysis (Wald-test) for the difference in the number of colonisation events (plant abundancies in treated plots) depending on species, plot-section, interaction between plot-section and species, date, TSLR: time since last vegetation removal and site. Effect
df
Chi2
p
Species Plot-section Plot-section *Species Date TSLR Site
4 1 4 3 1 3
35.34 21.27 12.5 51.32 3.53 41.92
<0.0001 <0.0001 0.014 <0.0001 0.060 <0.0001
while 11% was by fragments re-rooting. In the remaining 16% none of the previously hypothesized modes of colonisation could be ascertained. Germination of seeds or sprouting from turions or tubers was not observed at all during the study period. The species effect on colonisation mode was highly significant (Table 2). Colonisation by rhizomatic growth occurred mainly in P. perfoliatus, S. pectinata, where it formed 41% and 84% (respectively) of all colonisation events (Table 3). Both species used rhizomatic growth significantly more often than M. spicatum where it was only 3%. For M. spicatum the major strategy was colonisation by fragments (81%), which it used significantly more often than P. perfoliatus (31%). The differences between P. perfoliatus and M. spicatum colonisation strategies (distribution of rhizomatic growth, fragment rooting and unknown colonisation events) were significant for all months together (G = 76.2, Chi-squared df = 2, p < 0.01) and confirmed by separate tests for July-September, too. Composition of colonisation strategies were also significantly different
rhizome
fragment
unknown
total
0% 3% 13% 84% 41% 73%
100% 81% 88% 0% 31% 11%
0% 16% 0% 16% 28% 16%
1% 8% 3% 84% 5%
between S. pectinata and M. spicatum for all months (G = 808.3, Chi-squared df = 2, p < 0.01), and also confirmed by months tested separately (all differences at p < 0.01). “Unknown” events of colonisation might have resulted from overlooked tubers (of S. pectinata) or tiny seedlings (e.g. M. spicatum). Alternative strategies have been observed on P. perfoliatus and M. spicatum shoots (two times on each) which were still partly rooted, but intensely decomposing due to senescence and thereby weighed down by decomposing leaves, lying on the sediment surface. Formation of new healthy shoots was observed from these decaying shoots, often with fresh, adventitious roots. P. perfoliatus was also capable of forming lateral shoots from its (upright and healthy) stem with leaflets and adventitious roots and get established this way (once during the experiment). These events were registered as “unknown”, as they did not fall into any of the given categories. For investigating the importance of edges for colonisation, we tested differences between establishment in the outer section of each plot and the inner area (Table 4). The least squares mean estimations for the two sections and their geometric means ratios (GMRs, inner/outer) with corresponding 95% confidence intervals show that the outer parts were definitely more easily colonized by all species (Table 5). Establishment in the outer section of the plots was 2.4 times higher on average than in the inner areas. 4. Discussion The noted species proved to be highly successful in colonising newly created gaps in the vegetation. Characteristic strategies of the main macrophytic species in Lake Balaton could be identified in the presented field experiment, built of a species-specific set of several modes of reproduction and establishment. Life-history traits were often reflected in the single species‘ strategies. The observed establishment modes were almost exclusively based on fragment rooting and rhizomatic growth. Even though results of previous fragment-rooting laboratory experiments pointed towards the importance of this way of colonisation (BarratSegretain et al., 1999; Riis et al., 2009; Vári, 2013), it seemed less probable under natural and more adverse conditions, in water depths of up to 1.0 m. Fragment rooting was especially favoured by M. spicatum, whereas P. perfoliatus seemed to conduct a more mixed strategy, with a greater part of rhizomatic colonisation. Rhizomatic growth was the only way of colonisation detected for S. pectinata under in-situ experimental conditions (in agreement with Capers‘ (2003) observations), even though its potential to root from fragments had been proven in the laboratory (Vári, 2013) and studies describe it as predominantly propagating by tubers (Boedeltje et al., 2003; Van Wijk, 1989). Not only the best-known means of colonisation were observed. Additionally to the previously hypothesized colonisation modes, two more were detected which had not been expected or were never previously observed for these species: 1) re-growth from senescent, recumbent plants and 2) extension of lateral shoots with adventitious roots). Typically, the first process was observed at the
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Table 4 Colonisation events (plant densities per m2 ± SE) in the inner and outer section of plots for each colonising species and date. species
plot-section
date
Ceratophyllum demersum Myriophyllum spicatum
inner outer inner outer inner outer inner outer inner outer
07/07 0.1 0.6 2.2 ± 0.7 5.2 ± 1.4 0 0.2 12.4 ± 6.5 16.3 ± 8.5 0.4 ± 0.4 1.2 ± 0.4
Najas marina Stuckenia pectinata Potamogeton perfoliatus
03/08 0 0.2 0.9 ± 0.6 2.8 ± 0.6 0.3 ± 0.2 3.3 ± 3.1 11.2 ± 5.9 17.8 ± 9.1 0.4 ± 0.2 1.9 ± 0.7
10/09 0.1 0.1 0.1 1.9 ± 0.5 0.2 ± 0.0 0.7 ± 0.2 18.9 ± 11.3 60.9 ± 51.9 0.2 ± 0.0 2.3 ± 2.8
08/10 0.7 ± 1.0 1.4 ± 1.5 1.4 ± 0.2 1 ± 0.9 2.5 ± 0.5 9.1 ± 5.1 4.6 ± 1.7 10.4 ± 2.9 0.9 ± 0.5 1.1 ± 0.9
Table 5 Abundancies estimated in inner and outer sections with GEE model (least squares means, with 95% confidence intervals) and their geometric mean ratios (GMR with 95% confidence intervals) showing significance of differences. Species
Plot-section
observed N
Abundancy LSM (95% CI)
Ceratophyllum demersum Myriophyllum spicatum
outer inner outer inner outer inner outer inner outer inner
9 2 109 45 45 3 1055 471 65 18
0.1 (0.6–0.0) 0.0 (0.4–0.0) 1.2 (2.6–0.5) 0.5 (1.4–0.1) 0.4 (2.0–0.1) 0.0 (0.1–0.0) 12.0 (18.4–7.8) 5.5 (10.3–2.9) 0.7 (2.9–0.2) 0.2 (0.7–0.0)
Najas marina Stuckenia pectinata Potamogeton perfoliatus
end of the vegetation season. Re-sprouting from decaying plant material has been described before for S. pectinata and Potamogeton foliosus (Van Wijk, 1989; Yeo, 1966), but not yet for M. spicatum and P. perfoliatus. The concept of lateral shoots layering and rooting adventitiously is known from Wiegleb and Brux (1991) typology on broadleaved Potamogeton, and from Grace (1993) for emergent aquatic species (e.g. Ludwigia and Panicum), representing a mode for establishing new plantlets that is often disregarded. As expected, the importance of the surrounding vegetation for effective colonisation was also significant: the effect of adjacent vegetation on the edges was rather strong, even for non-rhizomatic species. This was demonstrated by the more than two-fold intensity of colonisation in the outer part of the plots. The importance of edges for re-establishment of certain aquatic species is also described in other studies for rivers and floodplains (Capers, 2003; Henry et al., 1996). Colonisation has strong seasonal dimensions, and is mostly governed by the plant’s phenology (Barrat-Segretain and Bornette, 2000): depending on the specific overwintering structures and the speed at which it develops biomass and propagules. There were three basic temporal patterns of colonisation observed for the different species. A colonisation peak in early summer was typical for the evergreen species, M. spicatum and C. demersum, with early growth and capacity to spread early in the year, followed by a smaller peak for M. spicatum in October, which is in compliance with most authors description of M. spicatum phenology (Aiken et al., 1979; Kimbel, 1982; Nichols and Shaw, 1986; Riis, 2008). In mid-summer (beginning of August), a peak of the annual species N. marina was observed, developing quickly in spring from seeds to great masses in summer. Van Viersen (1982) describes it as being dominant in late summer. N. marina is traditionally regarded as a rooting macrophyte (e.g. Handley and Davy, 2002), however in Lake Balaton we could observe it often de-rooted towards the end of summer, vital but rather fragile. While enhanced fragility suggests senescence towards the end of N. marina life-cycle (Källström et al.,
GMR (95% CI**)
0.18 (3.15–0.01) 0.39 (0.67–0.23) 0.04 (0.18–0.01) 0.46 (0.73–0.29) 0.27 (0.73–0.10)
2008; Grace, 1993), plants still succeeded in ripening seeds in this state. Fragile shoots possibly enhance seed distribution similarly to Zostera marina, where seed-bearing shoots become more fragile as seeds ripen (Källström et al., 2008) A late summer maximum colonisation, was typical for P. perfoliatus (as also stated by Riis, 2008) and S. pectinata (end of July, Kautsky, 1987), which mostly have to emerge in the spring from subterranean parts first, before they can colonize new areas. Several authors (Capers, 2003; Churchill, 1983; Wiegleb and Brux, 1991; Yeo, 1966) state an enhanced colonisation rate for submerged macrophytes in general at the end of the vegetative period in late summer or autumn, followed by a decline, which is in accordance with the species’ life history strategies. The timing of the experiment and of life-history events like turion sprouting might have prevented us from observing establishment from turions directly within the experiment. Turions, just as well as seeds are often mentioned germinating either in late autumn or in spring-early summer (e.g. Handley and Davy, 2005; Sastroutomo, 1981; Van Viersen, 1982; Van Wijk, 1989), during times which were not covered by the present experiment. While there was a variety of establishing modes and timing patterns in the present study, two major vegetative strategies – fragment rooting and rhizomatic growth – were predominant. All of them relied on neighbouring, already existent vegetation, which suggests that these vegetation patches have a great role in pioneering as cores from which re-establishment of vegetation can proceed on whole-lake level. Recovery of aquatic vegetation following large-scale vegetation loss (e.g. due to high eutrophication levels) often starts only slowly after trophic conditions returned to a favourable level (Bakker et al., 2012; Hilt et al., 2006; Jeppesen et al., 2005; Lauridsen et al., 2003), with possibly available remnant vegetation patches supporting the process (Sand-Jensen et al., 2008). However, in many cases neither is there enough vegetation left, nor are sufficient propagules stored in the sediment (seed and bud banks) for quick recolonisation. In these cases active plantings might be advisable in order to speed up the re-colonisation process
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Hobbs, W.O., Hobbs, J.M.R., LaFranc¸ois, T., Zimmer, K.D., Theissen, K.M., Edlund, M.B., Michelutti, N., Butler, M.G., Hanson, M.A., Carlson, T.J., 2012. A 200-year perspective on alternative stable state theory and lake management from a biomanipulated shallow lake. Ecol. Appl. 22, 1483–1496, http://dx.doi.org/10. 1890/11-1485.1. Istvánovics, V., Clement, A., Somlyódy, L., Specziár, A., G.-Tóth, L., Padisák, J., 2007. Updating water quality targets for shallow Lake Balaton (Hungary), recovering from eutrophication. Hydrobiologia 581, 305–318. Jeppesen, E., Søndergaard, M., Jensen, J.P., Havens, K.E., Anneville, O., Carvalho, L., Coveney, M.F., Deneke, R., Dokulil, M.T., Foy, B., Gerdeaux, D., Hampton, S.E., Hilt, S., Kangur, K., Köhler, J., Lammens, E.H. h. r., Lauridsen, T.L., Manca, M., Miracle, M.R., Moss, B., Nõges, P., Persson, G., Phillips, G., Portielje, R., Romo, S., Schelske, C.L., Straile, D., Tatrai, I., Willén, E., Winder, M., 2005. Lake responses to reduced nutrient loading—an analysis of contemporary long-term data from 35 case studies. Freshw. Biol. 50, 1747–1771, http://dx.doi.org/10.1111/j.13652427.2005.01415. x. Källström, B., Nyqvist, A., Aberg, P., Bodin, M., Andre, C., 2008. Seed rafting as a dispersal strategy for eelgrass (Zostera marina). Aquat. Bot. 88, 148–153. Kautsky, L., 1987. Life-cycles of three populations of Potamogeton pectinatus L. at different degrees of wave exposure in the Askö area northern Baltic Proper. Aquat. Bot. 27, 177–187. Kautsky, L., 1988. Life strategies of aquatic soft bottom macrophytes. Oikos 53, 126–135. Kimbel, J.C., 1982. Factors influencing potential intralake colonization by Myriophyllum spicatum L. Aquat. Bot. 14, 295–307. Lauridsen T.L., Jeppesen E., Sondergaard M., 1994. Colonization and succession of submerged macrophytes in shallow Lake Vaeng during the first five years following fish manipulation. Lauridsen, T.L., Jensen, J.P., Jeppesen, E., Sondergaard, M., 2003. Response of submerged macrophytes in Danish lakes to nutrient loading reductions and biomanipulation. Nichols, S.A., Shaw, B.H., 1986. Ecological life histories of the three aquatic nuisance plants, Myriophyllum spicatum, Potamogeton crispus and Elodea canadensis. Hydrobiologia 131, 3–21. Ozimek, T., 2006. The possibility of submerged macrophyte recovery from a propagule bank in the eutrophic Lake Mikołajskie (North Poland). Hydrobiologia 570, 127–131. Partridge, L., Harvey, P.H., 1988. The ecological context of life history evolution. Science 241, 1449–1455. R Developement Core Team, 2016. R: A language and environment for statistical computing. In: R Foundation for Statistical Computing (Vienna, Austria) https://www.R-project.org/. Riis, T., Madsen, T.V., Sennels, R.S.H., 2009. Regeneration, colonisation and growth rates of all ofragments in four common stream plants. Aquat. Bot. 90, 209–212. Riis, T., 2008. Dispersal and colonisation of plants in lowland streams: success rates and bottlenecks. Hydrobiologia 596, 341–351. Sand-Jensen, K., Pedersen, N.L., Thorsgaard, I., Moeslund, B., Borum, J., Brodersen, K.P., 2008. 100 years of vegetation decline and recovery in Lake Fure, Denmark. J. Ecol. 96, 260–271, http://dx.doi.org/10.1111/j.1365-2745.2007.01339. x. Sastroutomo, S.S., 1981. Turion formation, dormancy and germination of curly pondweed, Potamogeton crispus L. Aquat. Bot. 10, 161–173. Scheffer, M., Van Nes, E.H., 2007. Shallow lakes theory revisited: various alternative regimes driven by climate, nutrients, depth and lake size. Hydrobiologia 584, 455–466. Scheffer, M., 1990. Multiplicity of stable states in freshwater systems. Hydrobiologia 200, 475–486. Sculthorpe, C.D., 1967. The Biology of Aquatic Plants. Edward Arnold Ltd., London. Umetsu, C.A., Evangelista, H.B.A., Thomaz, S.M., 2012. The colonization, regeneration, and growth rates of macrophytes from fragments: a comparison between exotic and native submerged aquatic species. Aquat. Ecol. 46, 443–449, http://dx.doi.org/10.1007/s10452-012-9413-0. Vári, Á., 2013. Colonisation by fragments in six common aquatic macrophyte species. Fundam. Appl. Limnol. Arch. Für Hydrobiol. 183, 15–26, http://dx.doi. org/10.1127/1863-9135/2013/0328. Van Viersen, W., 1982. Some notes on the germination of seeds of Najas marina L. Aquat. Bot. 12, 201–203. Van Wijk, R.J., 1989. Ecological studies on Potamogeton pectinatus L. III. Reproductive strategies and germination ecology. Aquat. Bot. 33, 271–299. Wiegleb, G., Brux, H., 1991. Comparison of life history characters of broad-leaved species of the genus Potamogeton L. I. General characterization of morphology and reproductive strategies. Aquat. Bot. 39, 131–146. Yeo, R.R., 1966. Yields of propagules of certain aquatic plants I. Weeds 14, 110–113.
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Quantifying macrophyte colonisation strategies—A field experiment in a shallow lake (Lake Balaton, Hungary) Ágnes Vári ∗ , Viktor R. Tóth Balaton Limnological Institute, Centre for Ecological Research, Hungarian Academy of Sciences, 8237 Tihany, Klebelsberg K. u. 3, Hungary
a r t i c l e
i n f o
Article history: Received 11 October 2013 Received in revised form 12 September 2016 Accepted 15 September 2016 Available online 16 September 2016 Keywords: Regeneration Fragment rooting Rhizomatic growth Life-history Phenology Biomanipulation Lake recovery
a b s t r a c t Life-history traits like dominance of certain reproductive modes (e.g. vegetative, specialized, unspecialized or sexual propagules) and overwintering strategies (evergreen or re-sprouting) determine the success and timing of the ability of aquatic plants to colonize new areas. In the present experiment the distribution of these reproductive modes was examined in-situ, where new gaps were experimentally formed and establishment of new vegetation observed on a monthly bases in ten plots. During a period of 126 days, altogether 73% of all established plants (n = 1822) colonized by rhizomatic growth and 11% by rooting of vegetative fragments. Myriophyllum spicatum was observed to use mostly fragment rooting (81%), while Potamogeton perfoliatus followed a more mixed strategy combining re-rooting fragments and rhizomatic growth (31% and 41%, respectively). Stuckenia pectinata also preferred colonisation by rhizomes (84%). No colonisation by specialized vegetative units (tubers or turions) was observed during the study period The importance of surrounding vegetation was shown by comparing colonisation on inner and marginal sections of the plots (30% vs.70%). Three different patterns of timing of peak colonisation intensities were observed, related to species’ life-history traits. While several experimental works have been done on the regeneration and colonisation abilities of different species under laboratory conditions, information on the in-situ application of the different strategies is scarce. Insights on the modes by which plants succeed in colonising gaps helps us understand how (re)establishment of aquatic vegetation might function in lake ecosystems recovering after eutrophication. © 2016 Elsevier B.V. All rights reserved.
1. Introduction Plants, thus submerged aquatic macrophytes too, can propagate by both vegetative and sexual means. Macrophytes usually use a wider range of possible modes for establishing in new areas and in newly emerging patches than terrestrial plants do, thereby being able to colonize a diversity of habitats (Barrat-Segretain, 1996; Sculthorpe, 1967). This multiplicity of colonisation modes makes it possible to investigate the relationship between life-history traits (like different ways of reproduction) and colonisation success. Re-colonisation can occur on different spatial scales: locally, following either minor disturbance (such as strong currents or waves, which can dislocate bundles of plants, or feeding, trampling, boat movements), or major disturbance events, which eradicate
∗ Corresponding author. Present adress: Institute of Ecology and Botany, Centre for Ecological Research, Hungarian Academy of Sciences, 2163 Vácrátót, Alkotmány u. 2-4, Hungary. E-mail address: [email protected] (Á. Vári). http://dx.doi.org/10.1016/j.aquabot.2016.09.006 0304-3770/© 2016 Elsevier B.V. All rights reserved.
greater areas of aquatic vegetation (such as ice-scouring, drought or floods (Barrat-Segretain and Amoros, 1996; Kautsky, 1988), or at the whole lake-level, when a lake returns (through reoligotrophication) from algae-dominated turbid state that resulted from previous eutrophication (Scheffer, 1990; Scheffer and Van Nes, 2007). Re-establishment of macrophytic vegetation after return from high eutrophication levels is a common issue, especially in shallow lakes world-wide (excellent review by Bakker et al., 2012; Galanti et al., 1990; Hilt et al., 2010; Hobbs et al., 2012; Jeppesen et al., 2005; Lauridsen et al., 2003, 1994; Ozimek, 2006), as it is also in the study area Lake Balaton (Herodek et al., 1988; Istvánovics et al., 2007). This article argues that looking into details at the small scale might elucidate the potentials and limitations of processes on the large scale, whole-lake level. Colonisation by plants can be regarded as conquering new areas, establishing from propagules which arrived from other areas to that patch. Regeneration is seen as the process by which plants re-grow from some part of the whole plant, which might be below-ground or not (e.g. Barrat-Segretain et al., 1998; Umetsu et al., 2012). For the purpose of this study we defined (similarly to Capers, 2003
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and to Henry et al., 1996) all mechanisms of establishing new, aboveground canopy as colonisation, as they are all ways by which previously non-visible plants appear in the standing vegetation and can participate in further life-history events. Life history is composed of survival probabilities and rates of reproduction (Partridge and Harvey, 1988), including patterns of development, growth, reproduction and lifespan (Fabian and Flatt, 2012). The development of both vegetative and generative reproductive structures is determined by different life history traits and phenology, which in turn act on potential speed and timing of colonisation. Within the diversity of reproductive options open to a macrophyte, there are two major ways of reproduction, depending on whether a species overwinters solely as sexual propagules (as annuals do) or in some vegetative shape (like perennials). Overwintering in perennials can take place by receeding to underground plant parts, while some aquatic perennials remain partly green above-ground. The latter start in spring with a head start in developing biomass. Colonisation of newly available areas depends, apart from patch suitability, also on the surrounding vegetation within the waterbody, the effect of which is mostly detectable at the boundaries of gaps (e.g. Capers, 2003; Henry et al., 1996). Testing the effect of gap edges throws light on the importance of already existant macrophytic vegetation as kernels of (re)establishment. The set of reproductive options a species can resort to is delimited and timed by its life-history, whereas the relative importance with which the different colonisation modes are used also depends on the local environment (Capers, 2003; Wiegleb and Brux, 1991). However, it is expected that there are species-specific propagation strategies combining the available options in a characteristic way, but in lake ecosystems this has never before been quantified in-situ. Differences in the preference of colonisation modes might explain spatial as well as temporal patterns of macrophyte occurrence. Therefore, we wanted to investigate, a) whether different macrophyte species use different strategies in colonising and to quantify the propagation modes in relation to each other. In order to test the source of colonisation, we hypothesized that b) edge-effects would be strong, and c) there would be differences between the months in summer and autumn in colonisation intensities, relatable to the species life history traits.
2. Material and methods Ten plots of 1 m × 1 m were randomly designated in 0.6–1.0 m deep water in Lake Balaton (coordinates: 46◦ 54 50.26 N 17◦ 53 36.38 ) on 4th June 2009. Plots were arranged on four points (sub-sites), within a range of 5–70 m apart. The site represented the typical submerged vegetation of Lake Balaton with Potamogeton perfoliatus L., Stuckenia pectinata (L.) Böerner, Myriophyllum spicatum L., Ceratophyllum demersum L. and Najas marina L., belonging to the category of “Euhydrophyte vegetation of naturally eutrophic and mesotrophic still waters” in the national vegetation catalogue (Bölöni et al., 2011). At the start of the experiment, all vegetation was removed from the plots by hand, equipped with scuba diving gear, while care was taken to remove attached subterranean parts of the existent plants as completely as possible. We did not sift through the sediment in order to remove detached propagules, following the approach of Capers (2003). Plots, divided into a margin (outer 15 cm within the plot) and an inner section, were treated every 3–4 weeks (on 07/07, 03/08, 10/09 and 08/10) until the end of the vegetation period. Each time, all newly grown vegetation was carefully removed while checking whether it had established by one of the following colonisation modes suggested by Capers (2003) and own observations:
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1 by re-rooting of vegetative fragments (detectable by the blackened, slightly decomposing endings of a (half-buried) shoot) 2 by clonal (rhizomatic, lateral) growth from neighbouring plants (physical attachment to plants through their rhizomes outside the plot) 3 by re-sprouting of specialized vegetative propagules (turions or tubers) (recognizable by the remnants of the vegetative propagule that sprouted) Germination of seeds was not included in the assessment of the different colonisation modes as this probably mostly occurs during spring-time, which was not covered by the present study. If the colonisation event did not fall into any of the above categories, it was noted as “unknown”. C. demersum and N. marina fragments were often found on the plots without rooting, but as fragmentation and being unrooted belongs to their normal lifecycle, these events were counted as colonisation by fragments. In order to calculate colonisation potentials for the different species, plants were counted and species determined. In compliance with our definition of colonisation, each plant, possibly with several shoots or ramets that appeared on the treated plots was regarded as one colonisation event. This means that for C. demersum, which roots only with some minor rhizoids or not at all, colonisation was counted as such if any shoots were found lying on the sediment surface. The same applied for N. marina, which is also often found towards the end of the summer unrooted, seemingly without losing vitality. In order to take into account the correlated observations, generalized estimating equations (GEE) were applied with an assumed Poisson-distribution, implemented in SAS SAS University Edition, Version 2.2 (SAS/STAT). In order to control for potentially confounding effects, the GEE model included apart from species, plot-section (inner and outer) and date of sampling, also time since last vegetation removal (in days), interaction between species and plot-section as fixed effects and sampling site (A, B, C and D), as random effect. First order auto regressive covariance structure was used to describe the within plot error distribution. Fixed effects were tested at alpha level of 0.05 by means of Wald-test. Least squares mean estimations of abundancies in inner and outer plot sections and their geometric means ratios (GMRs, inner/outer) with corresponding Tukey – type 95% confidence intervals were derived. Differences between species in the distribution of colonisation modes were tested with G-test of independence in R version 3.2.2 for all months and for separate month too, in order to check results independently from date (R Developement Core Team, 2016). 3. Results A total of 1822 plants established during the whole research period from 7th June till 8th October (126 days), resulting in an overall colonisation rate of 1.4 plants per day per m2 . Most intense colonisation took place during August (peak value from harvesting on 7th September) with 85.1 ± 15.7 colonisation events per m2 on average (± SE), while it was lowest during the following month, harvested at the beginning of October (19.8 events ± 2.8). First it was M. spicatum and C. demersum which colonized most actively, during June (resulting in peak value sampled on 7th July), both declining steadily throughout the study period, with M. spicatum slightly increasing again in October (Fig. 1, Table 1). N. marina colonisation rates peaked next, in early August. In S. pectinata and P. perfoliatus most plants established during August, giving a maximum at the sampling on 10th September, exceeding plant densities of M. spicatum. Almost three quarters of all noted colonisation events (73%) could be assigned to rhizomatic growth from surrounding plants,
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Á. Vári, V.R. Tóth / Aquatic Botany 136 (2017) 56–60 Table 3 Colonisation modes used by the newly established species in the cleared plots in%. “rhizome” – rhizomatic growth, “fragment” – fragment rooting, “unknown” – could not be determined with certainty or was none of the hypothesized categories.
Ceratophyllum demersum Myriophyllum spicatum Najas marina Stuckenia pectinata Potamogeton perfoliatus total
Fig. 1. Colonisation events (plants per m2 ) for the species observed colonising experimentally de-vegetated plots during the study period in summer and autumn. Plants were summed up for each species and divided by 10 (=total area of clearance; number of plots) to get the mean plant densities/m2 . Note the second axis used for showing S. pectinata densities.
Table 1 Colonisation events (plant densities per m2 ± SE) in whole plots for each colonising species and date. Counted plants are summarized per species and date and divided by total area. species
Ceratophyllum demersum Myriophyllum spicatum Najas marina Potamogeton perfoliatus Stuckenia pectinata
date 07/07
03/08
10/09
08/10
0.7 7.4 ± 2.3 0.2 1.6 ± 0.6 28.7 ± 20.9
0.2 ± 2.5 3.7 ± 1.0 3.6 ± 4.5 2.3 ± 1.1 29.1 ± 18.1
0.2 2.0 ± 0.6 0.6 2.4 ± 5.5 79.9 ± 95.5
0 2.4 ± 1.6 0.4 ± 1.0 2.0 ± 1.2 15.0 ± 4.3
Table 2 Summary of GEE model fixed effects analysis (Wald-test) for the difference in the number of colonisation events (plant abundancies in treated plots) depending on species, plot-section, interaction between plot-section and species, date, TSLR: time since last vegetation removal and site. Effect
df
Chi2
p
Species Plot-section Plot-section *Species Date TSLR Site
4 1 4 3 1 3
35.34 21.27 12.5 51.32 3.53 41.92
<0.0001 <0.0001 0.014 <0.0001 0.060 <0.0001
while 11% was by fragments re-rooting. In the remaining 16% none of the previously hypothesized modes of colonisation could be ascertained. Germination of seeds or sprouting from turions or tubers was not observed at all during the study period. The species effect on colonisation mode was highly significant (Table 2). Colonisation by rhizomatic growth occurred mainly in P. perfoliatus, S. pectinata, where it formed 41% and 84% (respectively) of all colonisation events (Table 3). Both species used rhizomatic growth significantly more often than M. spicatum where it was only 3%. For M. spicatum the major strategy was colonisation by fragments (81%), which it used significantly more often than P. perfoliatus (31%). The differences between P. perfoliatus and M. spicatum colonisation strategies (distribution of rhizomatic growth, fragment rooting and unknown colonisation events) were significant for all months together (G = 76.2, Chi-squared df = 2, p < 0.01) and confirmed by separate tests for July-September, too. Composition of colonisation strategies were also significantly different
rhizome
fragment
unknown
total
0% 3% 13% 84% 41% 73%
100% 81% 88% 0% 31% 11%
0% 16% 0% 16% 28% 16%
1% 8% 3% 84% 5%
between S. pectinata and M. spicatum for all months (G = 808.3, Chi-squared df = 2, p < 0.01), and also confirmed by months tested separately (all differences at p < 0.01). “Unknown” events of colonisation might have resulted from overlooked tubers (of S. pectinata) or tiny seedlings (e.g. M. spicatum). Alternative strategies have been observed on P. perfoliatus and M. spicatum shoots (two times on each) which were still partly rooted, but intensely decomposing due to senescence and thereby weighed down by decomposing leaves, lying on the sediment surface. Formation of new healthy shoots was observed from these decaying shoots, often with fresh, adventitious roots. P. perfoliatus was also capable of forming lateral shoots from its (upright and healthy) stem with leaflets and adventitious roots and get established this way (once during the experiment). These events were registered as “unknown”, as they did not fall into any of the given categories. For investigating the importance of edges for colonisation, we tested differences between establishment in the outer section of each plot and the inner area (Table 4). The least squares mean estimations for the two sections and their geometric means ratios (GMRs, inner/outer) with corresponding 95% confidence intervals show that the outer parts were definitely more easily colonized by all species (Table 5). Establishment in the outer section of the plots was 2.4 times higher on average than in the inner areas. 4. Discussion The noted species proved to be highly successful in colonising newly created gaps in the vegetation. Characteristic strategies of the main macrophytic species in Lake Balaton could be identified in the presented field experiment, built of a species-specific set of several modes of reproduction and establishment. Life-history traits were often reflected in the single species‘ strategies. The observed establishment modes were almost exclusively based on fragment rooting and rhizomatic growth. Even though results of previous fragment-rooting laboratory experiments pointed towards the importance of this way of colonisation (BarratSegretain et al., 1999; Riis et al., 2009; Vári, 2013), it seemed less probable under natural and more adverse conditions, in water depths of up to 1.0 m. Fragment rooting was especially favoured by M. spicatum, whereas P. perfoliatus seemed to conduct a more mixed strategy, with a greater part of rhizomatic colonisation. Rhizomatic growth was the only way of colonisation detected for S. pectinata under in-situ experimental conditions (in agreement with Capers‘ (2003) observations), even though its potential to root from fragments had been proven in the laboratory (Vári, 2013) and studies describe it as predominantly propagating by tubers (Boedeltje et al., 2003; Van Wijk, 1989). Not only the best-known means of colonisation were observed. Additionally to the previously hypothesized colonisation modes, two more were detected which had not been expected or were never previously observed for these species: 1) re-growth from senescent, recumbent plants and 2) extension of lateral shoots with adventitious roots). Typically, the first process was observed at the
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Table 4 Colonisation events (plant densities per m2 ± SE) in the inner and outer section of plots for each colonising species and date. species
plot-section
date
Ceratophyllum demersum Myriophyllum spicatum
inner outer inner outer inner outer inner outer inner outer
07/07 0.1 0.6 2.2 ± 0.7 5.2 ± 1.4 0 0.2 12.4 ± 6.5 16.3 ± 8.5 0.4 ± 0.4 1.2 ± 0.4
Najas marina Stuckenia pectinata Potamogeton perfoliatus
03/08 0 0.2 0.9 ± 0.6 2.8 ± 0.6 0.3 ± 0.2 3.3 ± 3.1 11.2 ± 5.9 17.8 ± 9.1 0.4 ± 0.2 1.9 ± 0.7
10/09 0.1 0.1 0.1 1.9 ± 0.5 0.2 ± 0.0 0.7 ± 0.2 18.9 ± 11.3 60.9 ± 51.9 0.2 ± 0.0 2.3 ± 2.8
08/10 0.7 ± 1.0 1.4 ± 1.5 1.4 ± 0.2 1 ± 0.9 2.5 ± 0.5 9.1 ± 5.1 4.6 ± 1.7 10.4 ± 2.9 0.9 ± 0.5 1.1 ± 0.9
Table 5 Abundancies estimated in inner and outer sections with GEE model (least squares means, with 95% confidence intervals) and their geometric mean ratios (GMR with 95% confidence intervals) showing significance of differences. Species
Plot-section
observed N
Abundancy LSM (95% CI)
Ceratophyllum demersum Myriophyllum spicatum
outer inner outer inner outer inner outer inner outer inner
9 2 109 45 45 3 1055 471 65 18
0.1 (0.6–0.0) 0.0 (0.4–0.0) 1.2 (2.6–0.5) 0.5 (1.4–0.1) 0.4 (2.0–0.1) 0.0 (0.1–0.0) 12.0 (18.4–7.8) 5.5 (10.3–2.9) 0.7 (2.9–0.2) 0.2 (0.7–0.0)
Najas marina Stuckenia pectinata Potamogeton perfoliatus
end of the vegetation season. Re-sprouting from decaying plant material has been described before for S. pectinata and Potamogeton foliosus (Van Wijk, 1989; Yeo, 1966), but not yet for M. spicatum and P. perfoliatus. The concept of lateral shoots layering and rooting adventitiously is known from Wiegleb and Brux (1991) typology on broadleaved Potamogeton, and from Grace (1993) for emergent aquatic species (e.g. Ludwigia and Panicum), representing a mode for establishing new plantlets that is often disregarded. As expected, the importance of the surrounding vegetation for effective colonisation was also significant: the effect of adjacent vegetation on the edges was rather strong, even for non-rhizomatic species. This was demonstrated by the more than two-fold intensity of colonisation in the outer part of the plots. The importance of edges for re-establishment of certain aquatic species is also described in other studies for rivers and floodplains (Capers, 2003; Henry et al., 1996). Colonisation has strong seasonal dimensions, and is mostly governed by the plant’s phenology (Barrat-Segretain and Bornette, 2000): depending on the specific overwintering structures and the speed at which it develops biomass and propagules. There were three basic temporal patterns of colonisation observed for the different species. A colonisation peak in early summer was typical for the evergreen species, M. spicatum and C. demersum, with early growth and capacity to spread early in the year, followed by a smaller peak for M. spicatum in October, which is in compliance with most authors description of M. spicatum phenology (Aiken et al., 1979; Kimbel, 1982; Nichols and Shaw, 1986; Riis, 2008). In mid-summer (beginning of August), a peak of the annual species N. marina was observed, developing quickly in spring from seeds to great masses in summer. Van Viersen (1982) describes it as being dominant in late summer. N. marina is traditionally regarded as a rooting macrophyte (e.g. Handley and Davy, 2002), however in Lake Balaton we could observe it often de-rooted towards the end of summer, vital but rather fragile. While enhanced fragility suggests senescence towards the end of N. marina life-cycle (Källström et al.,
GMR (95% CI**)
0.18 (3.15–0.01) 0.39 (0.67–0.23) 0.04 (0.18–0.01) 0.46 (0.73–0.29) 0.27 (0.73–0.10)
2008; Grace, 1993), plants still succeeded in ripening seeds in this state. Fragile shoots possibly enhance seed distribution similarly to Zostera marina, where seed-bearing shoots become more fragile as seeds ripen (Källström et al., 2008) A late summer maximum colonisation, was typical for P. perfoliatus (as also stated by Riis, 2008) and S. pectinata (end of July, Kautsky, 1987), which mostly have to emerge in the spring from subterranean parts first, before they can colonize new areas. Several authors (Capers, 2003; Churchill, 1983; Wiegleb and Brux, 1991; Yeo, 1966) state an enhanced colonisation rate for submerged macrophytes in general at the end of the vegetative period in late summer or autumn, followed by a decline, which is in accordance with the species’ life history strategies. The timing of the experiment and of life-history events like turion sprouting might have prevented us from observing establishment from turions directly within the experiment. Turions, just as well as seeds are often mentioned germinating either in late autumn or in spring-early summer (e.g. Handley and Davy, 2005; Sastroutomo, 1981; Van Viersen, 1982; Van Wijk, 1989), during times which were not covered by the present experiment. While there was a variety of establishing modes and timing patterns in the present study, two major vegetative strategies – fragment rooting and rhizomatic growth – were predominant. All of them relied on neighbouring, already existent vegetation, which suggests that these vegetation patches have a great role in pioneering as cores from which re-establishment of vegetation can proceed on whole-lake level. Recovery of aquatic vegetation following large-scale vegetation loss (e.g. due to high eutrophication levels) often starts only slowly after trophic conditions returned to a favourable level (Bakker et al., 2012; Hilt et al., 2006; Jeppesen et al., 2005; Lauridsen et al., 2003), with possibly available remnant vegetation patches supporting the process (Sand-Jensen et al., 2008). However, in many cases neither is there enough vegetation left, nor are sufficient propagules stored in the sediment (seed and bud banks) for quick recolonisation. In these cases active plantings might be advisable in order to speed up the re-colonisation process
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