Respiration of turions and winter apices in aquatic carnivorous plants

Basic respiration characteristics were measured in turions of six aquatic plant species differing greatly in their ecological and overwintering characteristics both before and after overwintering, i.e., in dormant and non-dormant state: non-carnivorous Hydrocharis morsus-ranae and Caldesia parnassifolia and carnivorous Aldrovanda vesiculosa, Utricularia australis, U. ochroleuca, and U. bremii, and in non-dormant winter apices of three Australian (sub)tropical populations of Aldrovanda and of two temperate North American Utricularia species, U. purpurea and U. radiata. Respiration rate of autumnal (dormant) turions at 20°C ranged from 0.36 to 1.3 μmol O₂ kg⁻¹ (FM) s⁻¹ and, except for U. bremii, increased by 11–114% after overwintering. However, this increase was statistically significant only in two species. Respiration Q₁₀ in dormant turions ranged within 1.8–2.6 and within 2.3–3.4 in spring (non-dormant) turions. Turions of aquatic plants behave as typical storage, overwintering organs with low respiration rates. No relationship was found between respiration rate of turions and overwintering strategy. In spite of their low respiration rates, turions can usually survive only from one season to another, due to their limited reserves of respiratory substrates for long periods. Contrary to true turions, respiration rates in non-dormant winter apices both in Australian Aldrovanda populations and temperate U. radiata and U. purpurea, in sprouting turions, and growing shoot apices of Aldrovanda were high and ranged from 2.1 to 3.1 μmol kg⁻¹ (FM) s⁻¹, which is comparable to that in aquatic plant leaves or shoots.     

Seasonal growth dynamics and overwintering of the aquatic carnivorous plantAldrovanda vesiculosa at experimental field sites

New potential sites for the critically-endangered, aquatic carnivorous plantAldrovanda vesiculosa L. (Droseraceae) were selected in North and South Bohemia (Czech Republic) and both its seasonal growth dynamics and overwintering rate were investigated. Groups of either 5 or 10 plants were planted in 1×1 m nylon enclosures in selected shallow, dystrophic waters at the end of May. Plant growth characteristics and water chemistry were investigated at 2 to 5 week intervals over the 1994 growing season inside ten enclosures placed at six sites. Within seven enclosures at three sites, the seasonal growth was very fast and 38–141 turions developed from the initial five plants. Water at these sites was mesotrophic with a high concentration of CO₂ above 0.1 mmol.l^?1 and pH between 6.2 and 7.6. At the other three sites, plant growth was very poor. The fastest plant propagation was found between late June and mid-August and corresponded with the warmest seasonal period. During this period, the doubling time of the total number of shoot apices was 16.4–34.9 days. Turions developed in mid-September and sank to the bottom by mid-October. In some enclosures, the turions overwintered on the wet bottom whereas they were submersed in the other ones. Though the turions were subject to frosts of up to ?20°C, none died due to the frosts. Grazing of turions by ducks or small rodents was found at some sites. The overwintering rate of turions at sites varied from 0 to 70% and was not related to seasonal growth rate. Most turions floated to the surface and germinated during late April-early May. It is suggested that considerable turion losses in stable, naturalAldrovanda stands are compensated for by fast seasonal shoot growth and branching which leads to the recovery of an abundant plant population.     

Mineral cost of carnivory in aquatic carnivorous plants

Tissue N, P, K, Ca, and Mg content was estimated in traps and photosynthetic and carnivorous shoots in five aquatic carnivorous plant species from an outdoor culture: Aldrovanda vesiculosa, Utricularia vulgaris, U. reflexa, U. intermedia, and U. stygia, for the determination of the mineral cost of carnivory. In three species with monomorphic shoots (A. vesiculosa, U. vulgaris, U. reflexa), tissue P and K content in traps was significantly higher than that in their photosynthetic shoots, whereas N content was about the same. In U. stygia and U. intermedia with dimorphic shoots, tissue N and P content was markedly the highest in photosynthetic shoots followed by traps, while it was lowest in carnivorous shoots. In all five species, trap K content was significantly (2–4 times) higher than that in photosynthetic and carnivorous shoots. In all species, the values of the mineral cost of carnivory – the proportion of mineral nutrient amount contained in traps or carnivorous shoots to that in the total plant biomass – were within 19–61% for N, 33–76% P, 51–78% K, 26–70% Ca, and 34% for Mg. A new concept of the ecological cost-benefit relationships of plant carnivory, based on the mineral benefit of prey capture and mineral costs associated with trap production, is introduced for aquatic carnivorous plants. The evolution of this plant group is considered to show the optimization of these mineral cost-benefit relationships.     

Uniformity of organellar DNA in Aldrovanda vesiculosa, an endangered aquatic carnivorous species, distributed across four continents

Organellar DNA from the widely distributed but rare and critically endangered aquatic carnivorous plant Aldrovanda vesiculosa (Droseraceae) was examined. Six chloroplast intergenic regions (3700 nt in total) were sequenced before analyzing the Southern-RFLP (Restriction Fragment Length Polymorphism) of 2 mt gene flanking regions. Only two different chloroplast haplotypes among 15 A. vesiculosa accessions from Africa, Australia, Europe, and Japan were found, generally distinguishing European and non-European plants, with two exceptions. Genetic variation observed in A. vesiculosa appears to be even lower than in other aquatic species with a similar world-wide distribution. A recent bottleneck followed by long-distance dispersal by water birds or low mutation rates could be responsible for the observed genetic uniformity. Estimation of genetic distances based on six chloroplast intergenic regions led to the conclusion that the chloroplast genome of A. vesiculosa matches more closely to that of Drosera regia than Dionaea muscipula, a sister genus sharing snapping traps. The inconsistency between genetic distance estimates based on nuclear and cytoplasmic markers may reflect a chloroplast capture. In A. vesiculosa, a four amino acids substitution (TGWS) in the amino acid sequence of ATP synthase alpha subunit (ATP1), highly conserved mitochondrial protein, was discovered, unique among all organisms based on current knowledge.     

Micronutrient content does not reflect the status of health in the aquatic carnivorous plant <Emphasis Type="Italic">Aldrovanda vesiculosa</Emphasis>

Tissue micronutrient content (B, Fe, Mn, Zn, Cu, Mo, Co) was compared in healthy and ill shoots of a rootless aquatic carnivorous plant Aldrovanda vesiculosa growing in an outdoor culture, in plants in the field, in different accessions from around the world, and in shoots and turions. On the basis of microelemental analyses, the observed disorder of shoot apices cannot be explained as deficiency of any of the above micronutrients.     

Overwintering temperatures affect freezing temperatures of turions of aquatic plants

The effect of different overwintering temperatures (2.5 ± 1 °C in a refrigerator or outdoor natural overwintering on wet topsoil with weak frosts) on the freezing temperature and survival rate of turions of 10 aquatic plant species with different ecological traits (free-floating habit or bottom rooting) was studied using mini thermocouples. Dormant, non-hardened turions of 9 species exhibited freezing within a narrow temperature range of ?7.0 to ?10.2 °C, while Hydrocharis morsus-ranae froze at ?3.6 °C. The survival rate of the turions after the measurements was, however, very low (0–38%). In several species, the freezing temperature of turions at the beginning of germination was not significantly different (at p < 0.05) from the dormant ones. The mean freezing temperature of outdoor hardened turions of 6 species was within a very narrow range of ?2.8 to ?3.3 °C and was thus significantly higher by 4–7 °C (p < 0.0002) than that for the non-hardened turions. It is assumed that the freezing temperatures indicate freezing of the extracellular water. The hardened turions of all 7 species were able to survive mild winter frosts under the topsoil conditions at a rate of 76–100%. These characteristics suggest that the turions of aquatic species can be hardened by weak frosts and that their frost hardiness is based on the shift from frost avoidance in non-hardened turions to frost tolerance.     

Stay dormant or escape sprouting? Turion buoyancy and sprouting abilities of the submerged macrophyte Potamogeton crispus L.

The ability of asexual propagules to disperse is an important ecological determinant of the spread and establishment of many aquatic species. However, few previous studies have addressed the relationship between the asexual propagule buoyancy and sprouting abilities in submerged macrophytes. For this reason, turions of Potamogeton crispus samples were collected from Lake Liangzi, and an incubator sprouting experiment was conducted. Our results revealed that the floating turions showed higher sprouting rates than that of sinking turions, indicating the former ones are possibly with high levels of primary metabolites. The higher N and P concentrations in the floating turions caused lower C:N, C:P, and N:P ratios in these turions compared with sinking turions, which confirmed the activation of floating turions. The free amino acid and soluble carbohydrate concentrations were also higher in floating turions than those in sinking turions. Our results also revealed that turion leaf porosity rather than starch concentration may determine the density of P. crispus turions. This study makes a contribution to our understanding of how the internal characteristics of turions can (at least partly) determine dispersal outcomes and offers new insights into the dispersal and sprouting of asexual propagules of submerged macrophytes.     

The causes of sinking and floating in turions of Myriophyllum verticillatum

The sinking and floating (density) of the special winter buds (turions) produced by many aquatic plants play important roles in their life cycles, yet there has been little experimental study of these phenomena. However, it has been postulated that starch determines the density of turions. In order to test this hypothesis, turions of Myriophyllum verticillatum L. were collected from October through April and analyzed for density, dry-to-fresh-weight ratio and starch content. Density did not correlate closely (R² = 0.37) with the dry-to-fresh-weight ratios. Density strongly correlated (R² = 0.99) with starch only in the January collections, but not at several other times, so starch content alone is not always the major determinant of turion density. Intracellular lacunae (potentially gas spaces) also occur within the axes of these turions, and the lacunal volumes increased ca. 20-fold as they resumed growth, at which time the turions started to float. Significantly, turions, which were near the density of water, could be sunk or floated by changing the ambient pressure (which would alter their internal gas volume). Thus, starch has a role in determining the density of M. verticillatum turions, but the amount of intercellular gas space may be more important, especially when they resume growth in the spring.     

Population ecology of the endangered aquatic carnivorous macrophyte Aldrovanda vesiculosa at a naturalised site in North America

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Ecological requirements and recent European distribution of the aquatic carnivorous plantAldrovanda vesiculosa L.—A review

Aldrovanda vesiculosa, a critically endangered aquatic carnivorous plant, is a species rapidly vanishing from Europe. A map of its recent European distribution is given. Of its earlier distribution area covering a substantial part of Europe, only a few native sites in Hungary, Poland, Romania, Russia and Ukraine remain. On the basis of the literature, field research inAldrovanda habitats, and experience of its cultivation both in culture and in the field, its ecological requirements and habitat characteristics are reviewed. The most important requirements appear to be a high CO₂ concentration, a medium concentration of humic acids in the water, warm water of high transparency, and a very low biomass of accompanying aquatic plants. The possibility of forming new substitute localities ofAldrovanda is discussed.     

Ecophysiological Characterization of Dormancy States in Turions of the Aquatic Carnivorous Plant Aldrovanda vesiculosa

Two main dormancy states, innate and imposed dormancy, were characterized in turions (winter buds) of the aquatic carnivorous plant Aldrovanda vesiculosa L. (Droseraceae) kept at 3 ± 1 °C in a refrigerator over the winter. As a result of the breaking of imposed dormancy by a temperature increase (at 15 – 20 °C), some of the turions rose to the water surface within 1 – 3 d and germinated. Turion leaves contained large lacunae with a slimy reticulum and were filled by water over winter. As a result of breaking imposed dormancy, the proportion of gas volume in inner turion leaves rose from 10 – 20 % to 100 % of leaf lacunae volume. The aerobic dark respiration rate of the turions [0.74 – 1.5 μmol O₂) kg⁻¹(FM) s⁻¹] slightly increased during innate dormancy after 1 – 2 d at 20 °C, while it was almost constant during the breaking of imposed dormancy. The anaerobic fermentation rate of the turions was only 1.5 – 7 % of the oxygen respiration rate and also was constant during the breaking of imposed dormancy. In turions, the content of glucose, fructose, and sucrose was the same for the two states of dormancy, but starch content was greatly reduced for the imposed dormancy (10 – 11 vs. 32 % DM). It may be suggested that a temperature increase causes an increase of fermentation or respiration which is responsible for the evolution of gas in turion lacunae and, thus, for turion rising.     

Field growth characteristics of two aquatic carnivorous plants,Aldrovanda vesiculosa andUtricularia australis

Basic growth characteristics of two species of free-floating submerged carnivorous plants, the very rare and stenotopicAldrovanda vesiculosa and the very common and eurytopicUtricularia australis, were investigated in a 10/11-day field growth experiment within three nylon enclosures at two artificialAldrovanda sites in the T?eboň region, S Bohemia, Czech Republic, at the peak of a growing season. Growth ofAldrovanda was best at a meso-eutrophic site (biomass doubling time,T ₂, 8.4–10.7 days, mean growth of new leaf whorls 0.96 whorls days^?1, 1.6 developed branches per shoot) and slower at an oligo-mesotrophic site (T ₂ 17.2–21.5 days, growth of whorls 1.01 whorls days^?1, 0.1–0.5 branches per shoot). Growth ofUtricularia was similar at both sites (T ₂ 19.8–33.2 days or 9.1–16.8 days, growth of whorls 3.1 or 2.7 whorls days^?1, 1.5–2.1 or 0.8–1.4 developed branches per shoot at the former or latter site, respectively). Throughout the experiment, both species at the meso-eutrophic site allocated relatively more biomass to the production and growth of branches, than to that of new whorls. The results show thatAldrovanda, although usually considered as competitively weaker, can grow faster during the growing season peak thanUtricularia due to frequent branching and the subsequent rapid growth and separation of daughter shoots. Very rapid growth of rootless aquatic carnivorous plants in nutrient-poor habitats allows the consideration of ecophysiological adaptations that enable the plants to gain limiting mineral nutrients. These adaptations include carnivory, efficient nutrient reutilization from senescent shoots, and very high affinity for mineral nutrient uptake from water. Comparison of growth rates of rare and stenotopicA. vesiculosa and very common and eurytopicU. australis shows that differences in their rarity do not seem to be based on differences of growth rate.     

Seed reproductive biology of the rare aquatic carnivorous plant Aldrovanda vesiculosa (Droseraceae)

Despite the unprecedented global decline in extant populations of Aldrovanda vesiculosa in the last century, little is known about the reproductive biology of this iconic aquatic carnivorous plant. This study aimed to investigate the role of seed‐based reproduction in the ecology of A. vesiculosa, with particular focus on the interplay between the regulation of seed dormancy by temperature cues and the efficacy of exogenous ethylene gas to act as a germination stimulant, the desiccation capacity and long‐term storage potential of seeds for conservation purposes. Sexual reproduction appears to be extremely limited in both natural and naturalized populations across three continents, with high variability in the success of flowering and seed set between sites and between seasons. Overall, flowering yielded few fertile fruit (6–19% of flowers producing fertile fruit) and seed viability was variable but generally low (29–88%). Fecundity appears to be influenced by seasonal climatic conditions and microhabitat characteristics. Aldrovanda vesiculosa possesses physiologically dormant seeds, with germination stimulated by exposure to ethylene gas (>90% germination) at 25 °C. Seeds appear sensitive to desiccation and sub‐zero temperature storage, with no germination and markedly reduced embryo growth after storage of seeds for >1 month at 15 °C and 15% relative humidity or after short‐term (24 h) storage at ?18 °C. In the absence of significant conservation and restoration initiatives, the continuing decline of dystrophic freshwater wetland habitats globally leaves A. vesiculosa facing extinction. As the successful long‐term storage of seeds appears unfeasible based on the approaches described in this study, other alternatives for germplasm conservation such as cryostorage of vegetative tissues or zygotic embryos must be considered for establishing long‐term ex situ collections of critical germplasm.     

The molecular phylogeny of aquatic hyphomycetes with affinity to the Leotiomycetes

Aquatic hyphomycetes play a key role in decomposition of submerged organic matter and stream ecosystem functioning. We examined the phylogenetic relationships among various genera of aquatic hyphomycetes belonging to the Leotiomycetes (Ascomycota) using sequences of internal transcribed spacer (ITS) and large subunit (LSU) regions of rDNA generated from 42 pure cultures including 19 ex-types. These new sequence data were analyzed together with additional sequences from 36 aquatic hyphomycetes and 60 related fungi obtained from GenBank. Aquatic hyphomycetes, characterized by their tetraradiate or sigmoid conidia, were scattered in nine supported clades within the Helotiales (Leotiomycetes). Tricladium, Lemonniera, Articulospora, Anguillospora, Varicosporium, Filosporella, and Flagellospora are not monophyletic, with species from the same genus distributed among several major clades. The Gyoerffyella clade and the Hymenoscyphus clade accommodated species from eight and six different genera, respectively. Thirteen aquatic hyphomycete taxa were grouped in the Leotia-Bulgaria clade while twelve species clustered within the Hymenoscyphus clade along with several amphibious ascomycetes. Species of Filosporella and some species from four other aquatic genera were placed in the Ascocoryne-Hydrocina clade. It is evident that many aquatic hyphomycetes have relatives of terrestrial origin. Adaptation to colonize the aquatic environment has evolved independently in multiple phylogenetic lineages within the Leotiomycetes.     

Differential reliance on aquatic prey subsidies influences mercury exposure in riparian arachnids and songbirds

Cross‐ecosystem subsidies move substantial amounts of nutrients between ecosystems. Emergent aquatic insects are a particularly important prey source for riparian songbirds but may also move aquatic contaminants, such as mercury (Hg), to riparian food webs. While many studies focus on species that eat primarily emergent aquatic insects, we instead study riparian songbirds with flexible foraging strategies, exploiting both aquatic and terrestrial prey sources. The goal in this study is to trace reliance on aquatic prey sources and correlate it to Hg concentrations in common riparian arachnids (Families Tetragnathidae, Opiliones, and Salticidae) and songbirds (Common Yellowthroat Geothlypis trichas, Spotted Towhee Pipilo maculatus, Swainson''s Thrush Catharus ustulatus, Song Sparrow Melospiza melodia, and Yellow Warbler Setophaga petechia). We used stable isotopes of δ¹³C and δ¹⁵N and Bayesian mixing models in MixSIAR to determine the reliance of riparian predators on aquatic prey sources. Using mixed effects models, we found that arachnid families varied in their reliance on aquatic prey sources. While songbird species varied in their reliance on aquatic prey sources, songbirds sampled earlier in the season consistently relied more on aquatic prey sources than those sampled later in the season. For both arachnids and songbirds, we found a positive correlation between the amount of the aquatic prey source in their diet and their Hg concentrations. While the seasonal pulse of aquatic prey to terrestrial ecosystems is an important source of nutrients to riparian species, our results show that aquatic prey sources are linked with higher Hg exposure. For songbirds, reliance on aquatic prey sources early in the breeding season (and subsequent higher Hg exposure) coincides with timing of egg laying and development, both of which may be impacted by Hg exposure.     

Swan foraging shapes spatial distribution of two submerged plants,favouring the preferred prey species

Compared to terrestrial environments, grazing intensity on belowground plant parts may be particularly strong in aquatic environments, which may have great effects on plant-community structure. We observed that the submerged macrophyte, Potamogeton pectinatus, which mainly reproduces with tubers, often grows at intermediate water depth and that P. perfoliatus, which mainly reproduces with rhizomes and turions, grows in either shallow or deep water. One mechanism behind this distributional pattern may be that swans prefer to feed on P. pectinatus tubers at intermediate water depths. We hypothesised that when swans feed on tubers in the sediment, P. perfoliatus rhizomes and turions may be damaged by the uprooting, whereas the small round tubers of P. pectinatus that escaped herbivory may be more tolerant to this bioturbation. In spring 2000, we transplanted P. perfoliatus rhizomes into a P. pectinatus stand and followed growth in plots protected and unprotected, respectively, from bird foraging. Although swan foraging reduced tuber biomass in unprotected plots, leading to lower P. pectinatus density in spring 2001, this species grew well both in protected and unprotected plots later that summer. In contrast, swan grazing had a dramatic negative effect on P. perfoliatus that persisted throughout the summer of 2001, with close to no plants in the unprotected plots and high densities in the protected plots. Our results demonstrate that herbivorous waterbirds may play a crucial role in the distribution and prevalence of specific plant species. Furthermore, since their grazing benefitted their preferred food source, the interaction between swans and P. pectinatus may be classified as ecologically mutualistic.     

NaCl effect on the distribution of wall ingrowth polymers and arabinogalactan proteins in type A transfer cells of Medicago sativa Gabès leaves

In most species of the Genlisea–Utricularia sister lineage, the organs arising directly after germination comprise a single leaf-like structure, followed by a bladder-trap/stolon, with the lack of an embryonic primary root considered a synapomorphic character. Previous anatomical work suggests that the most common recent ancestor of Utricularia possessed an embryo comprising storage tissue and a meristematic apical region minus lateral organs. Studies of embryogenesis across the Utricularia lineage suggest that multiple primary organs have only evolved in the viviparous Utricularia nelumbifolia, Utricularia reniformis, and Utricularia humboldtii within the derived Iperua/Orchidioides clade. All three of these species are specialized for growth as “aquatic epiphytes” in the tanks of bromeliads, with recent phylogenetic evidence suggesting the possibility that multiple primary organs may have evolved twice independently within this clade. The primary organs of viviparous Utricularia also possess epidermal surface glands, and our study suggests that these may function as root hairs for uptake of solutes from the external environment—a possible adaptation for the “aquatic–epiphytic” habitat.     

Response of invasive macrophyte species to drawdown: The case of Elodea sp.

The response to drawdown of vegetative fragments (whole plants, shoot fragments and turions) of two invasive macrophyte species, Elodea canadensis and Elodea nuttallii, was studied through laboratory experiments. In addition, field observations were made on the colonisation of a wetland by E. nuttallii before and after a natural drawdown. The survival and the growth of vegetative fragments of E. nuttallii were higher than those of E. canadensis after an artificial drawdown of several days. In the field the recolonisation by E. nuttallii of a wetland that was drained for 10 weeks during a summer drawdown was very rapid, the abundance of this macrophyte species being not affected by the drawdown event. We conclude that E. nuttallii possesses a high resilience to desiccation and that a summer drawdown would not be efficient in the control of this invasive species.     

Water table and species identity outweigh carbon and nitrogen availability in a softwater plant community

Performance of aquatic macrophytes is driven by many environmental factors, and a major challenge is to understand how aquatic macrophyte communities are structured in various environments. In softwater lakes in Western Europe, hydrological state (submersed/emersed), carbon dioxide and ammonium levels and species interactions are considered as driving forces in structuring amphibious plant communities. In this study we aimed at evaluating the relative importance of these factors for four species in a competitive neighbourhood. Softwater lake habitat was simulated during one growing season in laboratory conditions, mimicking water level fluctuation, photoperiod and temperature. Artificial communities consisted of small populations of four softwater macrophyte species: Luronium natans, Baldellia ranunculoides ssp. repens, Eleocharis multicaulis and Hydrocotyle vulgaris. These communities were subjected to two levels of carbon dioxide and ammonium. Additionally, monocultures of Baldellia and Eleocharis were grown at a higher nutrient level combination in order to measure their competitive response in a community. Time (hydrological state) and species identity turned out to be the only consistently significant factors determining community composition. Plant performance was clearly species-dependent, while carbon dioxide and ammonium did not have major effects. The competitive response was significant in both Eleocharis and Baldellia. Competition intensity was highest in the emersed state. Carbon dioxide had a supplementary effect on the within-species performance in Luronium, Baldellia and Eleocharis, with high carbon dioxide level mainly resulting in more flowers and more stolons. Community outcomes and competitive responses in aquatic macrophytes appear difficult to predict, because of mixed life strategies and morphological and functional plasticity. We conclude that hydrological state was the only important environmental factor. The identity of the species that were present—implying species interactions—largely determined community outcome.     

Response of invasive macrophyte species to drawdown: The case of Elodea sp.

The response to drawdown of vegetative fragments (whole plants, shoot fragments and turions) of two invasive macrophyte species, Elodea canadensis and Elodea nuttallii, was studied through laboratory experiments. In addition, field observations were made on the colonisation of a wetland by E. nuttallii before and after a natural drawdown. The survival and the growth of vegetative fragments of E. nuttallii were higher than those of E. canadensis after an artificial drawdown of several days. In the field the recolonisation by E. nuttallii of a wetland that was drained for 10 weeks during a summer drawdown was very rapid, the abundance of this macrophyte species being not affected by the drawdown event. We conclude that E. nuttallii possesses a high resilience to desiccation and that a summer drawdown would not be efficient in the control of this invasive species.