The digestive systems of carnivorous plants.

To survive in the nutrient-poor habitats, carnivorous plants capture small organisms comprising complex substances not suitable for immediate reuse. The traps of carnivorous plants, which are analogous to the digestive systems of animals, are equipped with mechanisms for the breakdown and absorption of nutrients. Such capabilities have been acquired convergently over the past tens of millions of years in multiple angiosperm lineages by modifying plant-specific organs including leaves. The epidermis of carnivorous trap leaves bears groups of specialized cells called glands, which acquire substances from their prey via digestion and absorption. The digestive glands of carnivorous plants secrete mucilage, pitcher fluids, acids, and proteins, including digestive enzymes. The same (or morphologically distinct) glands then absorb the released compounds via various membrane transport proteins or endocytosis. Thus, these glands function in a manner similar to animal cells that are physiologically important in the digestive system, such as the parietal cells of the stomach and intestinal epithelial cells. Yet, carnivorous plants are equipped with strategies that deal with or incorporate plant-specific features, such as cell walls, epidermal cuticles, and phytohormones. In this review, we provide a systematic perspective on the digestive and absorptive capacity of convergently evolved carnivorous plants, with an emphasis on the forms and functions of glands.

Structural gradients and anisotropic hydraulic conductivity in the enigmatic eel traps of carnivorous corkscrew plants (Genlisea spp.).

PREMISE: Among the sophisticated trap types in carnivorous plants, the underground eel traps of corkskrew plants (Genlisea spp., Lentibulariaceae) are probably the least understood in terms of their functional principle. Here, we provide a detailed analysis of structural and hydraulic features of G. hispidula traps, contributing to the ongoing debate on whether these traps can actively generate water streams to promote prey capture. METHODS: Anatomical and hydraulic traits of detached traps, including inner trap diameters, chamber line element, hair length, glandular pattern, and hydraulic conductivity, were investigated quantitatively using light and electron microscopy, x-ray microtomography, and hydraulic measurements. RESULTS: Hydraulic resistivity in the neck of the trap, from the trap mouth toward the vesicle (digestive chamber) was 10 times lower than in the opposite direction. The comparison of measured and theoretical flow rates suggests that the retrorse hairs inside trap necks also provide considerable resistance against movement of matter toward the vesicle. Hairs showed a gradient in length along the neck, with the shortest hairs near the vesicle. Co-occurrence of quadrifid and bifid glands was limited to a small part of the neck, with quadrifids near the vesicle and bifids toward the trap mouth. CONCLUSIONS: The combination of structural gradients with hydraulic anisotropy suggests the trap is a highly fine-tuned system based on likely trade-offs between efficient prey movement in the trap interior toward the vesicle, prey retention, and spatial digestion capacities and is not counter to the generation of water streams.

High honeybee abundances reduce wild bee abundances on flowers in the city of Munich.

The increase in managed honeybees (Apis mellifera) in many European cities has unknown effects on the densities of wild bees through competition. To investigate this, we monitored honeybees and non-honeybees from 01 April to 31 July 2019 and 2020 at 29 species of plants representing diverse taxonomic and floral-functional types in a large urban garden in the city of Munich in which the same plant species were cultivated in both years. No bee hives were present in the focal garden, and all bee hives in the adjacent area were closely monitored by interviewing the relevant bee keepers in both 2019 and 2020. Honeybee numbers were similar in April of both years, but increased from May to July 2020 compared to 2019. The higher densities correlated with a significant increase in shifts from wild bee to honeybee visits in May/June/July, while visitor spectra in April 2019 and 2020 remained the same. Most of the species that experienced a shift to honeybee visits in 2020 were visited mostly or exclusively for their nectar. There were no shifts towards increased wild bee visits in any species. These results from a flower-rich garden have implications for the discussion of whether urban bee keeping might negatively impact wild bees. We found clear support that high honeybee densities result in exploitative competition at numerous types of flowers.

Measurement of the

We present a measurement of the low-energy (0-60 keV) γ-ray spectrum produced in the α decay of ^{233}U using a dedicated cryogenic magnetic microcalorimeter. The energy resolution of ∼10 eV, together with exceptional gain linearity, allows us to determine the energy of the low-lying isomeric state in ^{229}Th using four complementary evaluation schemes. The most precise scheme determines the ^{229}Th isomer energy to be 8.10(17) eV, corresponding to 153.1(32) nm, superseding in precision previous values based on γ spectroscopy, and agreeing with a recent measurement based on internal conversion electrons. We also measure branching ratios of the relevant excited states to be b_{29}=9.3(6)% and b_{42}<0.7%.

Changes in the bee fauna of a German botanical garden between 1997 and 2017, attributable to climate warming, not other parameters.

Botanical gardens represent artificial, but stable environments. With this premise, we analyzed the Munich Botanical Garden's bee fauna in 1997/1999 and again in 2015/2017. The garden covers 20 ha, uses no bee-relevant insecticides, has a protected layout, and on three sides abuts protected areas. Outdoors, it cultivates some 10,871 species/subspecies, many suitable as pollen and nectar sources for bees. The first survey found 79 species, the second 106, or 55% of the 192 species recorded for Munich since 1990. A Jackknife estimate for the second survey suggests 115 expected species. Classifying bees according to their thermal preferences (warm habitats, cool habitats, broad preferences, or unknown) revealed that 15 warm-loving species were gained (newly found), two lost (no longer found), and 12 retained, but only one cool-loving species was gained, three lost, and none retained, which multinomial models show to be significant differences. Of the 62 retained species, 27 changed in abundance, with 18 less frequent and nine more frequent by 2017 than they had been in 1997/1999. Retention, gain, or loss were unconnected to pollen specialization and Red List status of bee species. Between 1997 and 2017, average temperatures in Munich have increased by 0.5 °C, and climate warming over the past century is the most plausible explanation for the directional increase in warm-loving and the decrease in cool-adapted species. These results highlight the potential of botanic gardens with their artificially diverse and near-pesticide-free floras as systems in which to investigate climate change per se as a possible factor in shifting insect diversity.

Correction to: Changes in the bee fauna of a German botanical garden between 1997 and 2017, attributable to climate warming, not other parameters.

The same is included here.

Carnivorous leaves from Baltic amber.

The fossil record of carnivorous plants is very scarce and macrofossil evidence has been restricted to seeds of the extant aquatic genus Aldrovanda of the Droseraceae family. No case of carnivorous plant traps has so far been reported from the fossil record. Here, we present two angiosperm leaves enclosed in a piece of Eocene Baltic amber that share relevant morphological features with extant Roridulaceae, a carnivorous plant family that is today endemic to the Cape flora of South Africa. Modern Roridula species are unique among carnivorous plants as they digest prey in a complex mutualistic association in which the prey-derived nutrient uptake depends on heteropteran insects. As in extant Roridula, the fossil leaves possess two types of plant trichomes, including unicellular hairs and five size classes of multicellular stalked glands (or tentacles) with an apical pore. The apices of the narrow and perfectly tapered fossil leaves end in a single tentacle, as in both modern Roridula species. The glandular hairs of the fossils are restricted to the leaf margins and to the abaxial lamina, as in extant Roridula gorgonias. Our discovery supports current molecular age estimates for Roridulaceae and suggests a wide Eocene distribution of roridulid plants.

Evolution of genome size and chromosome number in the carnivorous plant genus Genlisea (Lentibulariaceae), with a new estimate of the minimum genome size in angiosperms.

BACKGROUND AND AIMS: Some species of Genlisea possess ultrasmall nuclear genomes, the smallest known among angiosperms, and some have been found to have chromosomes of diminutive size, which may explain why chromosome numbers and karyotypes are not known for the majority of species of the genus. However, other members of the genus do not possess ultrasmall genomes, nor do most taxa studied in related genera of the family or order. This study therefore examined the evolution of genome sizes and chromosome numbers in Genlisea in a phylogenetic context. The correlations of genome size with chromosome number and size, with the phylogeny of the group and with growth forms and habitats were also examined. METHODS: Nuclear genome sizes were measured from cultivated plant material for a comprehensive sampling of taxa, including nearly half of all species of Genlisea and representing all major lineages. Flow cytometric measurements were conducted in parallel in two laboratories in order to compare the consistency of different methods and controls. Chromosome counts were performed for the majority of taxa, comparing different staining techniques for the ultrasmall chromosomes. KEY RESULTS: Genome sizes of 15 taxa of Genlisea are presented and interpreted in a phylogenetic context. A high degree of congruence was found between genome size distribution and the major phylogenetic lineages. Ultrasmall genomes with 1C values of <100 Mbp were almost exclusively found in a derived lineage of South American species. The ancestral haploid chromosome number was inferred to be n = 8. Chromosome numbers in Genlisea ranged from 2n = 2x = 16 to 2n = 4x = 32. Ascendant dysploid series (2n = 36, 38) are documented for three derived taxa. The different ploidy levels corresponded to the two subgenera, but were not directly correlated to differences in genome size; the three different karyotype ranges mirrored the different sections of the genus. The smallest known plant genomes were not found in G. margaretae, as previously reported, but in G. tuberosa (1C ≈ 61 Mbp) and some strains of G. aurea (1C ≈ 64 Mbp). CONCLUSIONS: Genlisea is an ideal candidate model organism for the understanding of genome reduction as the genus includes species with both relatively large (∼1700 Mbp) and ultrasmall (∼61 Mbp) genomes. This comparative, phylogeny-based analysis of genome sizes and karyotypes in Genlisea provides essential data for selection of suitable species for comparative whole-genome analyses, as well as for further studies on both the molecular and cytogenetic basis of genome reduction in plants.

Distribution of Acetogenic Naphthoquinones in Droseraceae and Their Chemotaxonomic Utility.

Chemotaxonomy is the link between the state of the art in analytical chemistry and the systematic classification and phylogenetic analysis of biota. Although the characteristic secondary metabolites from diverse biotic sources have been used in pharmacology and biological systematics since the dawn of mankind, only comparatively recently established reproducible methods have allowed the precise identification and distinction of structurally similar compounds. Reliable, rapid screening methods like TLC (Thin Layer Chromatography) can be used to investigate sufficiently large numbers of samples for chemotaxonomic purposes. Using distribution patterns of mutually exclusive naphthoquinones, it is demonstrated in this review how a simple set of chemical data from a representative sample of closely related species in the sundew family (Droseraceae, Nepenthales) provides taxonomically and phylogenetically informative signal within the investigated group and beyond.

Training in medical communication competence through video-based e-learning: How effective are video modeling and video reflection?

OBJECTIVE: The present study investigated the efficacy of the didactic approaches of video modeling (VM, best-practice examples), video reflection (VR, problem-based approach), and the combination of both (VMR) in fostering medical communication competence in a video-based digital learning environment. METHODS: N = 126 third-year medical students who participated in the pre-post study were assigned to either the intervention groups (VM, VR, and VMR) or the wait-list control group. The efficacy of the three approaches was assessed by means of a situational judgment test (SJT) of medical communication competence. To investigate the differences between the wait-list control and the intervention groups (H1), between the single-mode and combined conditions (H2), and between VM and VR (H3), we applied planned contrast analyses. RESULTS: The planned contrasts showed that the VR condition significantly improved learning outcomes in comparison to the VM condition (H3). The decreased mean scores of the VM condition offset the increased mean scores of VR, and thus no significant differences could be found in H1 and H2. CONCLUSIONS: Our study provides promising evidence that VR fosters medical communication competence more effectively than VM. PRACTICAL IMPLICATIONS: Medical students' learning in video-based digital environments can be facilitated by the use of interactive VR.

Small Leaves, Big Diversity: Citizen Science and Taxonomic Revision Triples Species Number in the Carnivorous Drosera microphylla Complex (D. Section Ergaleium, Droseraceae).

The carnivorous Drosera microphylla complex from southwest Western Australia comprises a group of rare, narrowly endemic species that are potentially threatened by habitat destruction and illegal collection, thus highlighting a need for accurate taxonomic classification to facilitate conservation efforts. Following extensive fieldwork over two decades, detailed studies of both Australian and European herbaria and consideration of both crucial contributions by citizen scientists and social media observations, nine species of the D. microphylla complex are here described and illustrated, including four new species: D. atrata, D. hortiorum, D. koikyennuruff, and D. reflexa. The identities of the previously described infraspecific taxa D. calycina var. minor and D. microphylla var. macropetala are clarified. Both are here lectotypified, reinstated, and elevated to species rank. A replacement name, D. rubricalyx, is provided for the former taxon. Key morphological characters distinguishing the species of this complex include the presence or absence of axillary leaves, lamina shape, petal colour, filament shape, and style length. A detailed identification key, comparison figures, and a distribution map are provided. Six of the nine species are recommended for inclusion on the Priority Flora List under the Conservation Codes for Western Australian Flora and Fauna.

Dramatic difference in rate of chromosome number evolution among sundew (Drosera L., Droseraceae) lineages.

Chromosome number change is a driver of speciation in eukaryotic organisms. Carnivorous sundews in the plant genus Drosera L. exhibit single chromosome number variation both among and within species, especially in the Australian Drosera subg. Ergaleium D.C., potentially linked to atypical centromeres that span much of the length of the chromosomes. We critically reviewed the literature on chromosome counts in Drosera, verified the taxonomy and quality of the original counts, and reconstructed dated phylogenies. We used the BiChrom model to test whether rates of single chromosome number increase and decrease, and chromosome number doubling differed between D. subg. Ergaleium and the other subgenera and between self-compatible and self-incompatible lineages. The best model for chromosome evolution among subgenera had equal rates of chromosome number doubling but higher rates of single chromosome number change in D. subg. Ergaleium than in the other subgenera. Contrary to expectation, self-incompatible lineages had a significantly higher rate of single chromosome loss than self-compatible lineages. We found no evidence for an association between differences in single chromosome number changes and diploidization after polyploidy or centromere type. This study presents an exemplar for critically examining published cytological data and rigorously testing factors that may impact the rates of chromosome number evolution.

A novel approach for reliable qualitative and quantitative prey spectra identification of carnivorous plants combining DNA metabarcoding and macro photography.

Prey spectra (the number and composition of captured arthropods) represent a crucial aspect of carnivorous plant ecology, yet remain poorly studied. Traditional morphology-based approaches for prey identification are time-intensive, require specialists with considerable knowledge of arthropod taxonomy, and are hampered by high numbers of unidentifiable (i.e., heavily digested) prey items. We examined prey spectra of three species of closely-related annual Drosera (Droseraceae, sundews) from tropical northern Australia using a novel DNA metabarcoding approach with in-situ macro photography as a plausibility control and to facilitate prey quantity estimations. This new method facilitated accurate analyses of carnivorous plant prey spectra (even of heavily digested prey lacking characteristic morphological features) at a taxonomic resolution and level of completeness far exceeding morphology-based methods and approaching the 100% mark at arthropod order level. Although the three studied species exhibited significant differences in detected prey spectra, little prey specialisation was observed and habitat or plant population density variations were likely the main drivers of prey spectra dissimilarity.

Selecting the best candidates for resurrecting extinct-in-the-wild plants from herbaria.

Resurrecting extinct species is a fascinating and challenging idea for scientists and the general public. Whereas some theoretical progress has been made for animals, the resurrection of extinct plants (de-extinction sensu lato) is a relatively recently discussed topic. In this context, the term 'de-extinction' is used sensu lato to refer to the resurrection of 'extinct in the wild' species from seeds or tissues preserved in herbaria, as we acknowledge the current impossibility of knowing a priori whether a herbarium seed is alive and can germinate. In plants, this could be achieved by germinating or in vitro tissue-culturing old diaspores such as seeds or spores available in herbarium specimens. This paper reports the first list of plant de-extinction candidates based on the actual availability of seeds in herbarium specimens of globally extinct plants. We reviewed globally extinct seed plants using online resources and additional literature on national red lists, resulting in a list of 361 extinct taxa. We then proposed a method of prioritizing candidates for seed-plant de-extinction from diaspores found in herbarium specimens and complemented this with a phylogenetic approach to identify species that may maximize evolutionarily distinct features. Finally, combining data on seed storage behaviour and longevity, as well as specimen age in the novel 'best de-extinction candidate' score (DEXSCO), we identified 556 herbarium specimens belonging to 161 extinct species with available seeds. We expect that this list of de-extinction candidates and the novel approach to rank them will boost research efforts towards the first-ever plant de-extinction.

Snapshot prey spectrum analysis of the phylogenetically early-diverging carnivorous Utricularia multifida from U. section Polypompholyx (Lentibulariaceae).

Utricularia multifida is carnivorous bladderwort from Western Australia and belongs to a phylogenetically early-diverging lineage of the genus. We present a prey spectrum analysis resulting from a snapshot sampling of 17 traps-the first of this species to our knowledge. The most abundant prey groups were Ostracoda, Copepoda, and Cladocera. The genus cf. Cypretta (Cyprididae, Ostracoda) was the predominant prey. However, a high variety of other prey organisms with different taxonomic backgrounds was also detected. Our results indicate that U. multifida may potentially be specialized in capturing substrate-bound prey. Future approaches should sample plants from different localities to allow for robust comparative analyses.

Towards resolving Lamiales relationships: insights from rapidly evolving chloroplast sequences.

BACKGROUND: In the large angiosperm order Lamiales, a diverse array of highly specialized life strategies such as carnivory, parasitism, epiphytism, and desiccation tolerance occur, and some lineages possess drastically accelerated DNA substitutional rates or miniaturized genomes. However, understanding the evolution of these phenomena in the order, and clarifying borders of and relationships among lamialean families, has been hindered by largely unresolved trees in the past. RESULTS: Our analysis of the rapidly evolving trnK/matK, trnL-F and rps16 chloroplast regions enabled us to infer more precise phylogenetic hypotheses for the Lamiales. Relationships among the nine first-branching families in the Lamiales tree are now resolved with very strong support. Subsequent to Plocospermataceae, a clade consisting of Carlemanniaceae plus Oleaceae branches, followed by Tetrachondraceae and a newly inferred clade composed of Gesneriaceae plus Calceolariaceae, which is also supported by morphological characters. Plantaginaceae (incl. Gratioleae) and Scrophulariaceae are well separated in the backbone grade; Lamiaceae and Verbenaceae appear in distant clades, while the recently described Linderniaceae are confirmed to be monophyletic and in an isolated position. CONCLUSIONS: Confidence about deep nodes of the Lamiales tree is an important step towards understanding the evolutionary diversification of a major clade of flowering plants. The degree of resolution obtained here now provides a first opportunity to discuss the evolution of morphological and biochemical traits in Lamiales. The multiple independent evolution of the carnivorous syndrome, once in Lentibulariaceae and a second time in Byblidaceae, is strongly supported by all analyses and topological tests. The evolution of selected morphological characters such as flower symmetry is discussed. The addition of further sequence data from introns and spacers holds promise to eventually obtain a fully resolved plastid tree of Lamiales.

15N and 13C natural abundance of two mycoheterotrophic and a putative partially mycoheterotrophic species associated with arbuscular mycorrhizal fungi.

• In contrast to mycoheterotrophs that associate with ectomycorrhizal and saprotrophic fungi, we know little about the ecophysiology of arbuscular mycorrhizal mycoheterotrophs. Here, we identify the mycorrhizal fungi of two unrelated mycoheterotrophs and one putative partial mycoheterotroph that form arbuscular mycorrhizas, and analyse their carbon (C) and nitrogen (N) isotope signatures. • We used molecular methods to identify the mycorrhizal fungi of Dictyostega orobanchoides, Burmannia capitata (Burmanniaceae) and Voyria aphylla (Gentianaceae). Their C and N sources were investigated by analysing their stable isotope natural abundances (δ(13)C and δ(15)N). In addition, four putative partially mycoheterotrophic Burmannia species were grown ex situ. • We found that both mycoheterotrophs and a green Burmannia species are associated with nonoverlapping Glomeromycota fungi. The investigated mycoheterotrophs are significantly more enriched in (13)C than co-occurring autotrophic plants but lack significant (15)N enrichment. The green Burmannia species is not significantly enriched in (13)C and (15)N compared with surrounding plants and can grow fully autotrophically under controlled conditions. • Our results suggest that mycoheterotrophic Burmanniaceae and Gentianaceae are able to exploit arbuscular mycorrhizal fungi. Green relatives of mycoheterotrophic Burmanniaceae from high-light grassland sites also associate with arbuscular mycorrhizal fungi but we found no evidence that they receive detectable amounts of C from fungi.

Phylogenetics and character evolution in the carnivorous plant genus Genlisea A. St.-Hil. (Lentibulariaceae).

The carnivorous plant genus Genlisea A. St.-Hil. (Lentibulariaceae) comprises at least 22 species distributed in South and Central America as well as in Africa (including Madagascar). It has only recently been shown to be a true carnivore, specialized in protozoa and other small soil organisms. Here we present a statistically highly supported phylogeny of Genlisea based on three chloroplast loci. The most recent common ancestor of Genlisea most likely was of Neotropical origin and characterized by pedicels that are recurved in fruit, a strongly glandular inflorescence, and bivalvate capsule dehiscence. The further evolution of various morphological characters during the diversification of the genus is discussed. The two previously suggested subgenera Tayloria and Genlisea correspond to the two major clades found in our analyses. In subgenus Genlisea, three clades can be clearly distinguished based on molecular and morphological characters and on biogeographic patterns, which led us to propose a new sectional classification.

Development of a novel calorimetry setup based on metallic paramagnetic temperature sensors.

We have developed a new micro-fabricated platform for the measurement of the specific heat of low heat capacity mg-sized metallic samples, such as superconductors, down to temperatures of as low as 10 mK. It addresses challenging aspects of setups of this kind such as the thermal contact between the sample and platform, the thermometer resolution, and an addenda heat capacity exceeding that of the samples of interest (typically nJ/K at 20 mK). The setup allows us to use the relaxation method, where the thermal relaxation following a well defined heat pulse is monitored to extract the specific heat. The sample platform (5 × 5 mm2) includes a micro-structured paramagnetic Ag:Er temperature sensor, which is read out by a dc-superconducting quantum interference device via a superconducting flux transformer. In this way, a relative temperature precision of 30 nK/Hz can be reached, while the addenda heat capacity falls well below 0.5 nJ/K for T < 300 mK. A gold-coated mounting area (4.4 × 3 mm2) is included to improve the thermal contact between the sample and platform.

Hidden biodiversity of Amazonian white-sand ecosystems: two distinctive new species of Utricularia (Lentibulariaceae) from Pará, Brazil.

As deforestation and fire move forward over pristine vegetation in the Amazon, many species remain undiscovered and may be threatened with extinction before being described. Here, we describe two new species of Utricularia (Lentibulariaceae) collected during recent fieldwork in an area of white-sand vegetation in the eastern Amazon Basin named Campos do Ariramba. Further herbarium revision revealed that both species were first collected over 60 years ago in the same area, remaining unnamed until now. The new species, named U. ariramba sp. nov. and U. jaramacaru sp. nov., are placed in U. sect. Aranella and U. sect. Setiscapella, respectively. We provide full descriptions, illustrations, photographs, a distribution map, and taxonomic discussion for both species. Additionally, we provide a preliminary list of Lentibulariaceae from the Campos do Ariramba. Both new species are assessed as Vulnerable, however, yet known only from a few collections each, highlighting the urgency and importance of fieldwork and taxonomic revisions in the Amazon biogeographic region in order to provide essential data for the conservation of both known and still unknown biodiversity.