Only the adults survive – A long-term resistance of Isoëtes lacustris to acidity and aluminium toxicity stress in a Bohemian Forest lake

Highlights

• Acidic, aluminium-rich lake water damages sporeling absorptive organs in the sediment surface.

• Threshold dose-response relationships were found for sporeling rhizoids and the first root.

• Quillwort sporelings in vitro and in situ readily accumulate aluminium in their tissues.

• Lake acidification did not impair deeply rooted adults, which have survived for five decades.

Abstract

The aquatic quillwort Isoëtes lacustris L. survived five decades of severe acidification in Černé Lake (Bohemian Forest, central Europe), but failed to reproduce. To detect which ontogenetic stage is more affected by water acidification and to identify water chemistry thresholds for successful recruitment, experiments were carried out on quillwort sporelings grown in the laboratory, using different pH (4–8) and aluminium (Al) concentrations (0–1000 μg/L). Growth-related symptoms and Al accumulations in tissues were compared with those observed in sporelings collected in the lake. In the laboratory, the threshold Al concentrations ≥100 μg/L and pH ≤ 5.0 reduced absorptive organs (macrogametophyte rhizoids, roots, and root hairs), so that the ratio of below-ground to above-ground sporeling biomass decreased to <1. Nonetheless, stimulatory growth was demonstrated that affected the dose-response relationships of both absorptive and assimilative organs as well as sporeling growth restoration. The sporelings exposed to Al concentrations ≥100 μg/L accumulated high amounts of Al in their macrogametophytes and roots, but not in leaves. The lake sporelings had markedly longer roots, lower Al accumulations, but more reduced rhizoids and root hairs than those at 100 μg/L of Al in the laboratory. Even though water acidification was harmful to the shallow-rooted early ontogenetic stages, the in situ population survived due to the resistance and long life span of the deep-rooted adults. The effects of water acidification on sympatric congeneric quillworts as well as the other isoetids and competitive macrophytes in acid-sensitive softwater lakes are discussed, taking into account the influence of exposure to threshold acidity and Al toxicity and also the likelihood of such exposure.

Introduction

Many European softwater lakes were strongly affected by anthropogenic acidification due to atmospheric pollution with sulphur and nitrogen compounds in the second half of the 20th century, and experienced dramatic shifts in their original fauna and flora (Arts, 2002, Arts et al., 1990, Arts et al., 1989, Murphy, 2002, Rørslett and Brettum, 1989, Vrba et al., 2016, Roelofs et al., 1995). Thousands of these lakes that were originally dominated by small, slow-growing isoetid species with root-based nutrient uptake became dominated by relatively taller and fast-growing macrophytes with shoot-based nutrient uptake. These fast-growing canopy macrophytes were generally scattered among the original isoetid vegetation, but their growth was limited due to the oligotrophic conditions, which were largely a consequence of a presence of the isoetid plants themselves (i.e. through their high radial oxygen release controlling nutrient availability in the sediments; Smolders et al., 2002). Recently, lake water chemistry has largely reversed to preindustrial conditions due to reductions in acidic deposition (Evans et al., 2000). It remains unclear, however, whether (and to what extent) isoetid vegetation can recover (Baastrup-Spohr et al., 2017, Lucassen et al., 2016, Roelofs, 1983) and re-establish sustainable ecosystem functioning.

Here we show data on the recovery of the original flora in the Bohemian Forest lakes, the most strongly acidified and yet most rapidly recovering lakes worldwide (Evans et al., 2000, Vrba et al., 2016). Unlike other acidified European lake districts, the isoetids Isoëtes lacustris and Isoëtes echinospora Durieu survived in the Bohemian Forest lakes, rather than acidotolerant canopy species (e.g. Sphagnum spp. and Juncus bulbosus L.) (Čtvrtlíková et al., 2016, Čtvrtlíková et al., 2014). Moreover, there have been signs that these surviving sympatric congeneric isoetids differ substantially in their response to lake water recovery from acidification, providing a rare opportunity for understanding the responsiveness of the wider isoetid community. There is only limited evidence that isoetids vary in sensitivity to acidification (Rørslett and Brettum, 1989, Szmeja, 1994, Szmeja et al., 1997, Szmeja and Bociag, 2004, Vöge, 1997). Of the three originally dominant genera of isoetids in European lakes, Isoëtes spp. and Lobelia dortmanna L. have been substantially reduced in acidified lakes and are thus considered less tolerant than Littorella uniflora (L.) Asch. (Arts, 2002, Arts et al., 1989, Brouwer et al., 2002, Lucassen et al., 2016). However, particular symptoms of plant stress in these taxa have not yet been examined, even though each species has its own life strategy and tolerance limits. In addition, particular environmental factors vary both spatially and inter- and intraseasonally, and thus may act as stressors only in the species-specific period and environment of sensitive target organ development.

The effects of acidic deposition on water quality that are especially relevant to isoetid communities include reduced pH and associated increases in aluminium toxicity and/or ammonium concentration (e.g. Arts, 2002, Čtvrtlíková et al., 2009, Smolders et al., 2002). Ammonium is the preferred nitrogen form for taller macrophytes with predominantly shoot-based nutrient uptake such as Juncus bulbosus, Sphagnum spp. and other relatively common taxa currently displacing isoetids in acidified lakes (Smolders et al., 2002). Yet, the effects of ammonium elevation on macrophyte diversity have been stressed in the literature (Arts, 2002, Baastrup-Spohr et al., 2017, Smolders et al., 2002) while the direct phytotoxic effects of elevated aluminium or hydrogen ions on plant growth remain underexplored.

At pH ≤ 5.5 ionic aluminium forms (Al_i) dominate total Al concentrations in waters with low concentrations of dissolved organic carbon (DOC) (Stumm and Morgan, 1981). Al_i is a potent root toxicant for crop plants (Rout et al., 2001, Ma, 2007) but also for rooted aquatic macrophytes in lakes with acidified surface water (Čtvrtlíková et al., 2009). From our previous experimental study on Isoëtes echinospora, we presumed that Al_i would be detrimental especially to the shallow roots of the juvenile stages of submerged plants (Čtvrtlíková et al., 2016), since the deeper sediment horizons remain unaffected by lake water acidification and Al_i toxicity (Herlihy and Mills, 1986, Kopáček et al., 2001). In addition to starvation, these plantlets may also suffer from uprooting due to reduced root/shoot ratios (Čtvrtlíková et al., 2009). Once absorbed, Al_i is only slowly translocated within plant tissues and usually accumulates directly in the uptake organs (Dunbabin and Bowmer, 1992). Thus, these organs could be at high risk of time-cumulative Al_i toxicity (Poschenrieder et al., 2008). In addition to Al_i, excessive hydrogen ions may also compete with other cations for root absorption sites and disrupt their function. However, hydrogen ions were demonstrated to become toxic to roots only at pH < 3 (Bohn et al., 1979), but such a low pH was never found in the Bohemian Forest lakes even during the peak of acidification (Majer et al., 2003, Vrba et al., 2000).

As acid deposition in Europe decreases, acidification of softwater lakes tends to become less chronic and more episodic, but often a single acid episode can disrupt communities (Lovett et al., 2009). It is not yet clear to what extent episodic pH drops and extreme Al_i concentrations after high precipitation or snowmelt are critical for the recovery of isoetids. We have found that episodic increases in acidity and Al_i toxicity of the lake water during the early-summer disrupted the exclusively sexual reproductive cycle of Isoëtes echinospora by inhibiting the development of sporelings and long prevented population recovery in Plešné Lake (Bohemian Forest). Then, as the episodes of extreme acidity and Al_i toxicity became gradually restricted to the winter season, sporelings were able to fully develop in summer, and consequently a reproduction boom of I. echinospora in the lake was observed (Čtvrtlíková et al., 2016, Čtvrtlíková et al., 2012).

Surprisingly, the congeneric I. lacustris has not yet started recovery under very similar conditions in Černé Lake (Čtvrtlíková et al., 2014), with a monospecific plant stand of only adult plants present throughout several decades of lake acidification (Husák et al., 2000). This implies a similar scenario as for I. echinospora, i.e. that the acidic, Al-toxic lake water is detrimental to the fine absorptive organs of the sporelings developing at the sediment surface, rather than the deep-rooted adults. However, the recruitment success of I. lacustris might also be hindered by the synergistic effect of its very distinct phenology (Čtvrtlíková et al., 2014) and thus a distinct effective time for threshold acidity and Al_i stress. The lengthy germination and sporeling development of I. lacustris inevitably extend into the winter, when episodic extremes of pH and Al_i loadings might cause acute toxicity and prevent offspring survival. Alternatively, prolonged exposure to low-level stress in summer may cause cumulative poisoning by Al_i, if it is accumulated in plant tissues.

The general aim of this study was to elucidate to what extent I. lacustris and other competitive macrophytes suffer from lake water acidification, taking into account the effects of exposure to acidity and Al_i toxicity and also the likelihood of such exposure. The specific aims were (i) to assess water chemistry thresholds for the successful recruitment of the quillwort I. lacustris, (ii) to determine the effects of Al_i concentrations and water pH on the establishment and growth of sporelings of I. lacustris in laboratory experiments, (iii) to measure whether the sporelings accumulate Al_i in their tissues, and (iv) to examine sporelings from Černé Lake for symptoms of aluminium toxicity and compare them with sporelings grown in the laboratory.