Molecular Rates Parallel Diversification Contrasts between Carnivorous Plant Sister Lineages1

In the carnivorous plant family Lentibulariaceae, the bladderwort lineage (Utricularia and Genlisea) is substantially more species‐rich and morphologically divergent than its sister lineage, the butterworts (Pinguicula). Bladderworts have a relaxed body plan that has permitted the evolution of terrestrial, epiphytic, and aquatic forms that capture prey in intricately designed suction bladders or corkscrew‐shaped lobster‐pot traps. In contrast, the flypaper‐trapping butterworts maintain vegetative structures typical of angiosperms. We found that bladderwort genomes evolve significantly faster across seven loci (the trnL intron, the second trnL exon, the trnL–F intergenic spacer, the rps16 intron, rbcL, coxI, and 5.8S rDNA) representing all three genomic compartments. Generation time differences did not show a significant association. We relate these findings to the contested speciation rate hypothesis, which postulates a relationship between increased nucleotide substitution and increased cladogenesis.     

Prey spectra of aquatic Utricularia species (Lentibulariaceae) in northeastern Germany: The role of planktonic algae

The carnivorous bladderworts (Utricularia) possess complicated suction traps. Remarkably, information on the prey trapped is relatively sparse. We have conducted a detailed survey on the prey spectra found in traps of selected aquatic bladderworts (U. australis, U. vulgaris) occurring in ponds in northeastern Germany. A close examination of more than 200 traps revealed cladocerans, copepods, rotiferas, ciliates and insect larvae as being common prey.Of particular interest was the considerable amount of phytoplankton (i.e. algae, cyanobacteria) found in the traps. In total, more than 160 algae species (among others, Kirchneriella lunaris, Scenedesmus quadricauda and S. acuminatus) belonging to more than 50 genera were present, with Chlorophyceae being dominant. The role of the vegetarian diet for nutrient supply of bladderworts is discussed.     

Microbial community development in the traps of aquatic Utricularia species

We examined trap fluid of three aquatic carnivorous species of Utricularia (Lentibulariaceae) to assess the role of microbial community within their traps in plant nutrient acquisition. In the context of increasing trap age, we characterized microbial community composition using phospholipid fatty acid (PLFA) analysis and microscopy. Nutrient content in various fractions of the trap fluid was analyzed and the abundance of free-suspended bacteria estimated. The activities of extracellular phosphatase in the trap fluid were determined using fluorometry and the contribution of the microbial community to phosphatase production assessed by epifluorescence microscopy. The trap microbial community seems to be largely derived from Utricularia associated periphyton. PLFA analysis revealed that trap fluid contained all components of a complex microbial food web with bacteria forming more than 58% of the viable microbial biomass in the trap. Trap age seems to be the key factor in determining the patterns of microbial community development as well as enzyme production. The amount of nutrients increases with increasing trap age, and the total amounts of C, N, and P accumulated within traps during their lifetime are relatively large—of the order of 100 mg L⁻¹ for C and N, and between 0.2 and 0.6 mg L⁻¹ for P. A significant part of the nutrient pool is present in the dissolved form. Trap fluid stoichiometry (molar N:P ratios about 100) as well as the presence of nutrient limited microbial cells (molar N:P ratios 25–61) indicates the importance of phosphorus rather than nitrogen for the nutrition of Utricularia. Our findings support the hypothesis that mutualism, apart from the predator–prey interaction, is an important association in aquatic Utricularia traps and that the trap-associated microbial community may be of benefit to the rootless aquatic Utricularia species facing problems with P acquisition due to the loss of roots in their evolution.     

<Emphasis Type="Italic">Utricularia</Emphasis>: a vegetarian carnivorous plant?

Aquatic carnivorous plants of the genus Utricularia capture and utilise a wide range of small aquatic organisms. Most of the literature focuses on animals as prey. In this study, we investigate the occurrence of algae inside the traps of four species of bladderwort. We observed that algae of 45 genera form up to 80% of the total prey; algae were found frequently in traps without animal prey. The majority are coccal and trichal algae of the families Desmidiaceae and Zygnemataceae. The percentage of algae increases significantly with decreasing electric conductivity of the water (r _S = −0.417; P = 0,000). Thus, algae are the most frequent prey in extremely soft waters. The percentage of algae did not differ significantly, not within the investigated Utricularia species or within the various study sites. However, the taxonomic composition of the algal prey showed highly significant differences between different sites. More than 90% of the trapped algae were killed and degraded by the bladders. The recent data allow for two alternative hypotheses: either algal prey supplements animal prey in oligotrophic waters, or the unprofitable trapping of algae is rather an additional stress factor for Utricularia and contributes to its limited distribution in some peat bogs.     

The role of phytoplankton in the diet of the bladderwort Utricularia australis R.Br. (Lentibulariaceae)

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Functional characteristics of traps of aquatic carnivorous Utricularia species

Firing and resetting of traps in aquatic Utricularia species are associated with water flow and trap volume changes. In this study, trap thickness was used as a measure of water flow and was monitored automatically using an electronic position sensor. The basic characteristics of mechanically stimulated firing and resetting were measured in isolated traps from 13 aquatic Utricularia species and in two trap size categories in Utricularia reflexa. This allowed to study the relationship between these trap functions and trap thickness and length (criteria of trap size). Additionally, the characteristics of spontaneous firings (without any mechanical stimulation) were compared for U. reflexa traps fed or denied prey during a 1-day period. On the absolute scale, the 13 Utricularia species differed considerably in their firing and resetting rates. Significant interspecific differences were also found in the magnitude of firing (in total 3.7–4.2 times) and resetting rates (10–24 times) per unit trap thickness or length. Overall, traps of Utricularia australis, Utricularia stellaris and Utricularia inflata showed the greatest firing and resetting rates. The relative magnitude of firing per unit trap thickness or length showed a highly significant negative correlation with both trap thickness and length and the same also held for the relative resetting rates. Smaller and narrower traps are thus relatively more effective at trap firing and resetting than larger traps. Neither firing nor resetting characteristics were significantly different between unfed and prey-fed traps of U. reflexa and this was also true for the occurrence of spontaneous firings. A strict linear resetting rate, without any lag-period, was found during the first 3 min after trap firing in U. reflexa. This suggests that water is pumped out of the trap continuously and probably recirculates. Given the concepts of spontaneous firing and water recirculation, an ecological model based on the literature data has been devised to quantify the daily N and P gain from the ambient water by Utricularia traps devoid of animal prey. The model shows that the total N and P content estimated in the trap fluid is too high to be accumulated from only the ambient water. This implies that the prey-free traps do not take up N or P from the trap fluid but rather exude a quantity of these nutrients to the fluid to support the microbial community. Therefore, the trap microorganisms behave more as parasites than commensals and represent an additional ecological cost for trap maintenance.     

Dark respiration of leaves and traps of terrestrial carnivorous plants: are there greater energetic costs in traps?

In this study, O₂-based dark respiration rate (R_D) in leaf and trap cuttings was compared in 9 terrestrial carnivorous plant species of 5 genera to decide whether traps represent a greater energetic (maintanence) cost than leaves or photosynthetic parts of traps. R_D values of cut strips of traps or leaves of terrestrial carnivorous plants submerged in water ranged between 2.2 and 8.4 nmol g⁻¹ s⁻¹ (per unit dry weight) in pitcher traps of the genera Sarracenia, Nepenthes, and Cephalotus, while between 7.2 and 25 nmol g⁻¹ _DW s⁻¹ in fly-paper or snapping traps or leaves of Dionaea and Drosera. No clear relationship between R_D values of traps (or pitcher walls) and leaves (or pitcher wings or petioles) was found. However, RD values of separated Drosera prolifera tentacles exceeded those of leaf lamina 7.3 times.     

Ecological Traits of the Algae‐Bearing Tetrahymena utriculariae (Ciliophora) from Traps of the Aquatic Carnivorous Plant Utricularia reflexa

Trap fluid of aquatic carnivorous plants of the genus Utricularia hosts specific microbiomes consisting of commensal pro‐ and eukaryotes of largely unknown ecology. We examined the characteristics and dynamics of bacteria and the three dominant eukaryotes, i.e. the algae‐bearing ciliate Tetrahymena utriculariae (Ciliophora), a green flagellate Euglena agilis (Euglenophyta), and the alga Scenedesmus alternans (Chlorophyta), associated with the traps of Utricularia reflexa. Our study focused on ecological traits and life strategies of the highly abundant ciliate whose biomass by far exceeds that of other eukaryotes and bacteria independent of the trap age. The ciliate was the only bacterivore in the traps, driving rapid turnover of bacterial standing stock. However, given the large size of the ciliate and the cell‐specific uptake rates of bacteria we estimated that bacterivory alone would likely be insufficient to support its apparent rapid growth in traps. We suggest that mixotrophy based on algal symbionts contributes significantly to the diet and survival strategy of the ciliate in the extreme (anaerobic, low pH) trap‐fluid environment. We propose a revised concept of major microbial interactions in the trap fluid where ciliate bacterivory plays a central role in regeneration of nutrients bound in rapidly growing bacterial biomass.     

不同生境自交植物黄花大苞姜生殖分配的研究

为了探讨自交植物黄花大苞姜(Caulokaempferia coenobialis)对石壁附生这一特殊生境的生态适应,对其不同物候期和不同生境的生殖分配进行了对比研究。结果表明,在生殖生长过程中,黄花大苞姜种群用于营养生长的生物量分配占有绝对优势,而用于生殖的生物量分配比例较小(<13%)。在黄花大苞姜各构件的生物量分配中,根茎和叶的比重较大(24.22%~43.25%)。在光线较弱生境中的种群,为了提高资源获取能力,黄花大苞姜分配到叶的比重明显高于光线较强的种群,而分配给根茎的比例却明显低于光线较强的种群。随着物候期的推移,黄花大苞姜生殖分配的比例不断增加,到果期达到最大值。不同种群间和年度间黄花大苞姜分配给生殖构件的比例没有显著差异,推测其生殖分配可能受遗传因素控制。个体大小与根茎生物量呈极显著线性函数同速生长,而与生殖分配在云天海种群没有表现出相关性,在上坪和天堂顶种群表现为同速生长关系,但决定系数小于40%。因此,黄花大苞姜能有效调节其在不同生境的生物量分配以适应石壁附生的特殊生境,在光线较弱的种群提高叶的生物量分配并降低根茎的生物量分配以提高资源的获取能力。整体上投资到营养构件的生物量占比高达87%以上,生殖构件在居群间和年度间均保持稳定。这种繁殖策略,一方面较高的营养构件投资可以获得更多的资源,另一方面稳定的生殖投资可以保证种群的延续,各构件相互协调以更好适应石壁这一资源匮乏的生境。     

Trap gland morphology and its systematic implications in Taiwan Utricularia (Lentibulariaceae)

The highly specialized trap glands of carnivorous plant are responsible for the digestion and absorption of the prey; however, there are few studies on their systematics and evolution. In this study, the gland morphology of six carnivorous plant species of the genus Utricularia (Lentibulariaceae) in Taiwan, including U. aurea Lour., U. australis R. Br., U. bifida L., U. caerulea L., U. gibba L. and U. striatula Sm., was examined with a scanning electron microscope. The glands on both the outer and inner surfaces of the traps were examined. We found that the external glands had little diagnostic value, but the internal glands could be used in the identification of Taiwan species. Evolutionary trends of gland characteristics are discussed, analyzing morphology of the internal glands, based on previous work. A new hypothesis for the evolution of internal gland structure in Utricularia is also proposed.     

Compensation and Plasticity in an Invasive Plant Species

Plant plasticity under varying resources is one character that contributes to competitiveness and invasibility. The plasticity of plant modules of the invasive Japanese stilt grass (Microstegium vimineum) was examined under different light and nutrient levels using a balanced field and greenhouse study. Ample light and nutrients resulted in the greatest biomass accumulation in all plant modules. However, M. vimineum showed extreme plasticity, producing stolons and flowers (reproductive structures) under a wide range of environmental conditions except infertile, low light. The addition of nutrients under various shading regimes compensated for lower light levels, rendering little change in the allocation of carbon to reproductive structures. Data from the field study corroborate the greenhouse results, but also suggest plasticity in response to competition.     

The comparison of mechanically stimulated and spontaneous firings in traps of aquatic carnivorous Utricularia species

Firing and resetting of traps in aquatic Utricularia species are associated with water flows and trap volume changes. In this study, trap thickness was used as a measure of water flow and was monitored automatically using an electronic position sensor. Isolated traps from three aquatic Utricularia species were monitored over the course of 1-2 days to verify spontaneous firings (without any mechanical stimulation) and describe their basic characteristics. Isolated traps of three Utricularia species were initially fired by mechanical stimulation and allowed to naturally reset within a period of 24-48 h. Within this resting period, spontaneous firings were found in the traps of all species and in two trap age categories of U. vulgaris. The timing of spontaneous firings was found to be irregular. Spontaneous firings ranged between 0.29 and 2.4 during the 24-h resting period and the mean time between two spontaneous firings was highly variable within each species (319-891 min). There was no quantitative difference between spontaneous and mechanically stimulated firings of the traps. Spontaneous firings could explain how phytoplankton or detritus enters traps even when no prey species are present.     

Open dichotomous venation in the leaves ofUtricularia striatula (Lentibulariaceae)

The open dichotomous pattern of venation in the leaves ofUtricularia striatula is described in detail and compared withCircaeaster andKingdonia. Similar traits of dichotomous venation occur in other species ofUtricularia and may be due to reduction.Studies on IndianUtricularia, 3.     

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.     

Photosynthesis and dark respiration of leaves of terrestrial carnivorous plants

Using CO₂ gasometry, net photosynthetic (P _N) and dark respiration rates (R _D) were measured in leaves or traps of 12 terrestrial carnivorous plant species usually grown in the shade. Generally, mean maximum P _N (60 nmol CO₂ g⁻¹(DM) s⁻¹ or 2.7 μmol m⁻² s⁻¹) was low in comparison with that of vascular non-carnivorous plants but was slightly higher than that reported elsewhere for carnivorous plants. After light saturation, the facultatively heliophytic plants behaved as shade-adapted plants. Mean R _D in leaves and traps of all species reached about 50% of maximum P _N and represents the high photosynthetic (metabolic) cost of carnivory.     

Density-dependent reproductive and vegetative allocation in the aquatic plant Pistia stratiotes (Araceae)

Pistia stratiotes is an aquatic macrophyte that grows in temporary-ponds in the southern Pantanal, Brazil. It reproduces both sexually and asexually and is usually observed forming dense mats on the water surface, a condition favored by the plant's vegetative reproduction coupled with an ability for rapid growth. In this study we examined the effect of densely crowded conditions on the production of reproductive and vegetative structures. In addition, we verified whether there is a trade-off between clonal growth and investment in sexual reproductive structures, and whether there is an allocation pattern with plant size. Individual plant biomass and the number of the rosettes producing sexual reproductive structures and vegetative growth structures both increased with density. Increase in plant size resulted in increased proportional allocation to sexual reproductive structures and vegetative growth structures. Allocation of biomass to reproduction did not occur at the expense of clonal growth. Thus, the density response appears as a increase of rosettes producing sexual reproductive structures and vegetative growth structures. Therefore, long leaves and stolons may be adaptive under densely crowded conditions where competition for light is intense. An important aspect in the study of trade-offs is the size-dependency of the allocation patterns .Usually, larger plants produce more biomass. Therefore, larger plants can allocate more biomass to both vegetative and sexual reproduction than smaller plants and thus show a positive correlation between both traits rather than the expected negative one.     

Anatomical studies on seeds and seedlings of some Utricularia (Lentibulariaceae)

The undifferentiated mature embryos of someUtricularia studied consist of large polygonal cells which contain many starch grains. Later, they consist mostly of large polygonal cells with some small cells in one or more regions adjacent to the seed coat, which lack starch grains but have rather easily visible nuclei. After these small cells divide and produce more cells of the same type toward the midcenter of the embryo, they form one or more primordia which grow into the primary structures of the seedling. The primordia of the embryo seem to have no pattern as to which primary vegetative structure they will develop into. However, the terrestrial species ofUtricularia studied showed some non-cotyledonous, primary differences in germination patterns; some form primary foliar units, some form stolons, and some form bladders. The first and second primary foliar units of aquaticUtricularia radiata andV. gibba subsp.gibba do not follow in the same manner as cotyledons. No cotyledon could be distinguished in any of theUtricularia seedlings studied. In the seedlings ofU. gibba subsp.gibba andU. radiata, appearance and differentiation of the vascular elements occur simultaneously in more than one direction, toward the meristematic tissues of primary vegetative structures and toward the midcenter of the embryos. Lloyd’s proposed term: “cotyledonoids” (1942) and that of Kumazawa: “cotyledons” (1967) should not be used for the first and second primary foliar units in either aquatic or terrestrial to terrestrial-epiphyticUtricularia, unless further supportive evidence is accumulated.     

Ecophysiological characterization of carnivorous plant roots: Oxygen fluxes,respiration, and water exudation

Various ecophysiological investigations on carnivorous plants in wet soils are presented. Radial oxygen loss from roots of Droseraceae to an anoxic medium was relatively low 0.02 – 0.07 mol(O₂) m^{– 2} s^–1 in the apical zone, while values of about one order of magnitude greater were found in both Sarracenia rubra roots and Genlisea violacea traps. Aerobic respiration rates were in the range of 1.6 – 5.6 mol kg^–1 (f.m.) s^–1 for apical root segments of seven carnivorous plant species and 0.4 – 1.1 mol kg^–1 (f.m.) s^–1 for Genlisea traps. The rate of anaerobic fermentation in roots of two Drosera species was only 5 – 14 % of the aerobic respiration. Neither 0.2 mM NaN₃ nor 0.5 mM KCN influenced respiration rate of roots and traps. In all species, the proportion of cyanide-resistant respiration was high and amounted to 65 – 89 % of the total value. Mean rates of water exudation from excised roots of 12 species ranged between 0.4 – 336 mm 3 kg^–1 (f.m.) s^–1 with the highest values being found in the Droseraceae. Exudation from roots was insensitive to respiration inhibitors. No significant difference was found between exudation rates from roots growing in situ in anoxic soil and those kept in an aerated aquatic medium. Carnivorous plant roots appear to be physiologically very active and well adapted to endure permanent soil anoxia.     

Fluorescence labelling of phosphatase activity in digestive glands of carnivorous plants

Abstract: A new ELF (enzyme labelled fluorescence) assay was applied to detect phosphatase activity in glandular structures of 47 carnivorous plant species, especially Lentibulariaceae, in order to understand their digestive activities. We address the following questions: (1) Are phosphatases produced by the plants and/or by inhabitants of the traps? (2) Which type of hairs/glands is involved in the production of phosphatases? (3) Is this phosphatase production a common feature among carnivorous plants or is it restricted to evolutionarily advanced species? Our results showed activity of the phosphatases in glandular structures of the majority of the plants tested, both from the greenhouse and from sterile culture. In addition, extracellular phosphatases can also be produced by trap inhabitants. In Utricularia, activity of phosphatase was detected in internal glands of 27 species from both primitive and advanced sections and different ecological groups. Further positive reactions were found in Genlisea, Pinguicula, Aldrovanda, Dionaea, Drosera, Drosophyllum, Nepenthes, and Cephalotus. In Utricularia and Genlisea, enzymatic secretion was independent of stimulation by prey. Byblis and Roridula are usually considered as “proto‐carnivores”, lacking digestive enzymes. However, we found high activity of phosphatases in both species. Thus, they should be classified as true carnivores. We suggest that the inflorescence of Byblis and some Pinguicula species might also be an additional “carnivorous organ”, which can trap a prey, digest it, and finally absorb available nutrients.