Hypericum foliosum

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Habitus and growth type

Life span: Perennial

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Life span
Life span categories reflect the length of life duration of individual species. Annual plants finish their life cycle within one growing season. Biennial or short-lived plants are overwintering, growing only vegetatively in the first season and fruiting in the following season/s. Most of them are monocarpic, i.e. they finish their life cycle after producing fruits. Perennial plants can stay in vegetative form for several seasons, repeatedly flower and produce seeds (polycarpic strategy). Some species were assigned to more than one category because of their different life span in different parts of Europe, e.g., annual life span in northern Europe and biennial or short-lived life span in the Mediterranean.

The data were compiled from Klotz et al. 2002, Săvulescu (1952-76) and complemented by additional sources such as national and regional floras. If possible we used also the life form assessment to decide the life span category.

Categories

Annual

Biennial or short-lived

Perennial

Data source and citation

Dřevojan, P., Čeplová, N., Štěpánková, P., & Axmanová, I. (2023). Life span. – www.FloraVeg.EU.

Further references

Klotz, S., Kühn, I. & Durka, W. (2002). BIOLFLOR – Eine Datenbank zu biologisch-ökologischen Merkmalen der Gefäßpflanzen in Deutschland. Schriftenreihe für Vegetationskunde, 38, 1–334.
Săvulescu, T. (Ed.) (1952–1976). Flora Republicii Populare Române – Flora Republicii Socialiste România. Vols 1–13. București: Editura Academiei Republicii Populare Române, Academia Republicii Socialiste România.
Life form: Phanerophyte, Shrub

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Life form
The main categories of the life-form classification follow the system of Raunkiaer (1934), which is based on the position of the buds that survive the unfavourable season. In addition, we use auxiliary categories where it is possible to use finer differentiation.

At least one main category is assigned to each species, while some species can belong to more than one main category. Phanerophyte is a perennial woody or succulent plant with regenerative buds higher than 30 cm above the soil surface (includes trees, shrubs and tall succulents, excludes lianas and epiphytes). Chamaephyte is a perennial herb, low woody plant or succulent with regenerative buds above ground level, but not taller than 30 cm (includes dwarf shrubs, semi-shrubs, small succulents and some herbs). Hemicryptophyte is a perennial or biennial herb with regenerative buds on shoots at the ground level. Geophyte is a perennial plant with regenerative buds located belowground, usually with bulbs, tubers, or rhizomes. Hydrophyte is a plant that survives unfavourable seasons by means of buds that are at the bottom of a water body. Therophyte is a summer- or winter-annual herb that survives adverse seasons only as seeds and germinates in autumn, winter or spring. Epiphyte is either parasitic or non-parasitic plant that grows on other plants.

Auxiliary categories are only used for some species. Tree is a phanerophyte with a stem and a crown. Shrub is a phanerophyte branching from the stem base. Woody liana is a phanerophyte in the form of a long-stemmed woody vine. Semi-shrub (i.e. suffruticose chamaephyte) is a chamaephyte with shoots that usually grow straight up, bear leaves and flowers and die at the end of the growing season except for their lower part, which bears buds. Dwarf shrub is a chamaephyte with shoots that lignify instead of dying. Herbaceous liana is a hemicryptophyte, geophyte or therophyte with climbing aboveground stems.

Data were compiled from several databases and floras (Săvulescu 1952–1976, Horváth et al. 1995, Klotz et al. 2002, Tavşanoğlu & Pausas 2018, Guarino et al. 2019, Kaplan et al. 2019, French Flora database), European broad-scale studies (Wagner et al. 2017, Giulio et al. 2020), and different online sources (e.g. GreekFlora.gr). In the case of different assessments in original data sources, we critically revised them using additional sources.

Categories

Phanerophyte

Chamaephyte

Hemicryptophyte

Geophyte

Hydrophyte

Therophyte

Epiphyte

Tree

Shrub

Woody liana

Semi-shrub

Dwarf shrub

Herbaceous liana

Data source and citation

Dřevojan, P., Čeplová, N., Štěpánková, P., & Axmanová, I. (2023) Life form. – www.FloraVeg.EU.

Further references

Giulio, S., Acosta, A. T. R., Carboni, M., Campos, J. A., Chytrý, M., Loidi, J., … Marcenò, C. (2020). Alien flora across European coastal dunes. Applied Vegetation Science, 23(3), 317–327. https://doi.org/10.1111/avsc.12490
GreekFlora.gr. Available at https://www.greekflora.gr/ [accessed June 2020]
Guarino, R., La Rosa, M. & Pignatti, S. (Eds) (2019). Flora d'Italia, volume 4. Bologna: Edagricole.
Horváth, F., Dobolyi, Z. K., Morschhauser, T., Lõkös, L., Karas, L. & Szerdahelyi, T. (1995). Flóra adatbázis 1.2 – taxonlista és attribútum-állomány. [FLORA database 1.2 – lists of taxa and relevant attributes.] Vácrátót: FLÓRA munkacsoport, MTA-ÖBKI, MTM Növénytára.
French Flora database (baseflor), project of Flore et végétation de la France et du Monde: CATMINAT. Available at http://philippe.julve.pagesperso-orange.fr/catminat.htm [accessed June 2020]
Kaplan Z., Danihelka J., Chrtek J. Jr., Kirschner J., Kubát K., Štěpánek J. & Štech M. (Eds.) (2019). Klíč ke květeně České republiky [Key to the flora of the Czech Republic]. Ed. 2. Praha: Academia.
Klotz, S., Kühn, I. & Durka, W. (2002). BIOLFLOR – Eine Datenbank zu biologisch-ökologischen Merkmalen der Gefäßpflanzen in Deutschland. Schriftenreihe für Vegetationskunde, 38, 1–334.
Raunkiaer C. (1934). The life forms of plants and statistical plant geography. Oxford: Clarendon Press.
Tavşanoğlu, Ç., & Pausas, J. (2018). A functional trait database for Mediterranean Basin plants. Scientific Data, 5, 180135. https://doi.org/10.1038/sdata.2018.135
Wagner, V., Chytrý, M., Jiménez-Alfaro, B., Pergl, J., Hennekens, S., Biurrun, I., … Pyšek, P. (2017). Alien plant invasions in European woodlands. Diversity and Distributions, 23(9), 969–981. https://doi.org/10.1111/ddi.12592
Săvulescu, T. (Ed.) (1952–1976). Flora Republicii Populare Române – Flora Republicii Socialiste România. Vols 1–13. București: Editura Academiei Republicii Populare Române, Academia Republicii Socialiste România.

Fruit, seed and dispersal

Seed mass [mg]: 0.07

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Seed mass

Seed mass represent the mean weight of 1000 seeds in a dry state, measured in grams. The data were taken preferably from Kleyer et al. (2008), Hintze et al. (2013), García-Gutiérrez et al. (2018) and Seed Information Database (Royal Botanic Gardens Kew 2021) and complemented by additional sources such as national and regional floras. Each species is characterized by a mean value calculated across available datasets. Upon request, minimum, maximum and median values are also available.

Data source and citation

Axmanová, I. (2022). Seed mass. – www.FloraVeg.EU.

Further references

García-Gutiérrez, T., Jiménez-Alfaro, B., Fernández-Pascual, E., & Müller, J. V. (2018). Functional diversity and ecological requirements of alpine vegetation types in a biogeographical transition zone. Phytocoenologia, 77–89. https://doi.org/10.1127/phyto/2017/0224
Hintze, C., Heydel, F., Hoppe, C., Cunze, S., König, A., & Tackenberg, O. (2013). D3: The Dispersal and Diaspore Database – Baseline data and statistics on seed dispersal. Perspectives in Plant Ecology, Evolution and Systematics, 15(3), 180–192. https://doi.org/10.1016/j.ppees.2013.02.001
Kleyer, M., Bekker, R. M., Knevel, I. C., Bakker, J. P., Thompson, K., Sonnenschein, M., … Peco, B. (2008). The LEDA Traitbase: A database of life-history traits of the Northwest European flora. Journal of Ecology, 96(6), 1266–1274. https://doi.org/10.1111/j.1365-2745.2008.01430.x
Royal Botanic Gardens Kew. (2021). Seed Information Database (SID). Version 7.1. Available at: http://data.kew.org/sid/ [accessed May 2021]
Dispersal mode: Local non-specific dispersal

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Dispersal mode
Dispersal mode (dispersal syndrome, dispersal type) characterizes plant dispersal ability. It is represented by following categories: (i) local non-specific dispersal, which combines self-dispersal (autochory) and dispersal initiated by wind, where diaspores do not have any efficient special dispersal features, including several dispersal modes (namely ballochory, blastochory, boleochory, barochory); (ii) myrmecochory (ant dispersal); (iii) wind dispersal (anemochory), diaspores have special dispersal features such as hem, pappus, trichomes, dusty seeds or the species are tumbleweeds; (iv) animal dispersal includes dyszoochory, i.e. diaspores foraged by animals, which sometimes hide them as stock; (v) endozoochory, i.e. dispersal in animal gastrointestinal tract, and (vi) epizoochory, i.e., dispersal of diaspores attached on animal fur; special case is the (vii) anthropochory, i.e. human dispersal and (viii) hydrochory (water dispersal). Please note that hydrochory is not considered in the dispersal distance classes classification.

The dispersal modes are mainly estimated from species' morphological characteristics.

Categories

Local non-specific dispersal

Myrmecochory

Anemochory

Dyszoochory

Endozoochory

Epizoochory

Anthropochory

Hydrochory

Data source and citation

Lososová Z., Axmanová I., Chytrý M., Midolo G., Abdulhak S., Karger D.N., Renaud J., Van Es J., Vittoz P. & Thuiller W. (2023). Seed dispersal distance classes and dispersal modes for the European flora. Global Ecology and Biogeography, 32(9), 1485–1494.

Further references

Vittoz P. & Engler R. (2007). Seed dispersal distances: a typology based on dispersal modes and plant traits. Botanica Helvetica, 117, 109–124.
Dispersal distance class: 2

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Dispersal distance class
Dispersal distance classes are represented by ordered classes from 1 to 7, where classes 1 to 6 represent a gradient from short-distance dispersal to long-scale dispersal. The last class represents the dispersal mediated by humans. For species of the last class the assignment to the previous six classes and natural dispersal mode are given. The assignment of individual plants follows Lososová et al. (2023), a dataset prepared using the adjusted methodology of Vittoz & Engler (2007).

To assign plants into dispersal distance classes, several plant characteristics were obtained from various sources, namely plant height, life form, predominant dispersal mode, seed mass, typical habitat, plant geographical origin and information on dispersal by humans. In contrast to the original approach of Vittoz & Engler (2007), definitions of the dispersal distance classes were slightly modified.

Class 1 contains species shorter than 0.3 m. Their seeds do not have any specific dispersal features. Species are mostly self-dispersed, although seed dispersal can be initiated by wind, e.g., by shaking the fruit, which causes the diaspore to fall down. Class 2 is the most species-rich, including species with non-specific local dispersal strategy taller than 0.3 m. Class 3 includes ant-dispersed (myrmecochorous) species and wind-dispersed (anemochorous) forest herbs and dwarf shrubs. Class 4 is the least species-rich, including less efficient wind-dispersed woody plants and tumbleweeds. Class 5 includes wind-dispersed herbs and shrubs of open habitats and wind-dispersed trees with more efficient dispersal units (with trichomes). Class 6 includes species with different modes of animal dispersal. They can be dyszoochorous (i.e., foraged by animals, which sometimes hide them as stock), endozoochorous (i.e., dispersal in animal gastrointestinal tract), and epizoochorous (i.e., dispersal on animal fur). Finally, class 7 contains human-dispersed (antropochorous) species.

The species of the last class are also classified into one of the previous six classes based on their natural dispersal mode. Only classes 1-6 can be used in studies at the landscape scale where it is assumed that most species disperse naturally. All seven classes can be used in studies at a broader geographical scale where rare events of long-distance human dispersal are important.

Classes

Class 1. Small plants without any specific dispersal features. Mean dispersal distance: 0.1–1 m.

Class 2. Tall plants without any specific dispersal features. Mean dispersal distance: 1–5 m.

Class 3. Wind-dispersed plants of forest understorey and ant-dispersed plants. Mean dispersal distance: 2–15 m.

Class 4. Tumbleweed and wind dispersed trees and shrubs without trichomes. Mean dispersal distance: 40–150 m.

Class 5. Wind dispersed trees and shrubs with trichomes and wind dispersal plants of open habitats. Mean dispersal distance: 10–500 m.

Class 6. Animal dispersed plants. Mean dispersal distance: 400–1500 m.

Class 7. Human dispersed plants. Mean dispersal distance: 500 –5000 m.

Data source and citation

Lososová Z., Axmanová I., Chytrý M., Midolo G., Abdulhak S., Karger D.N., Renaud J., Van Es J., Vittoz P. & Thuiller W. (2023). Seed dispersal distance classes and dispersal modes for the European flora. Global Ecology and Biogeography, 32(9), 1485–1494.

Further references

Vittoz P. & Engler R. (2007). Seed dispersal distances: a typology based on dispersal modes and plant traits. Botanica Helvetica, 117, 109–124.

Trophic mode

Parasitism and mycoheterotrophy: autotroph

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Parasitism and mycoheterotrophy
In plant parasitism, two groups can be distinguished based on two different mechanisms. The first group of parasitic plants includes those directly parasitizing on another plant. These plants are called haustorial parasites. Using a specialized organ, the haustorium, they attach themselves to other plants and uptake resources from the host’s vascular bundles. The second group comprises mycoheterotrophic plants, which parasitise fungi via mycorrhizal interactions and gain organic carbon from them. Plants in both groups display variable dependence on their host organism.

The functional categorization of parasitic plants has been a topic of an active debate that is still ongoing. The traditional categories are based on the ability to perform photosynthesis (photosynthetic hemiparasites and non-green holoparasites) and the location of the haustoria (root and stem parasites) (Heide-Jørgensen 2008). However, such a classification system struggles with phenomena such as rudimentary photosynthesis in some species, variable photosynthetic activity throughout the life cycle, and the existence of parasitic plants that integrate with their host to such an extent that they can be considered endophytic. For the functional classification of European parasitic plants, we have adopted the most recent classification system proposed by Teixeira-Costa & Davis (2021) with small further modifications. This system relies primarily on ontogenetic development and strategies of attachment to the host. The values of other important functional traits, including photosynthetic capacity, type of vascular bundle connection, development of the primary haustorium, and location of haustoria on the host are also well discriminated by the categories of Teixeira-Costa & Davis (2021).

Euphytoid hemiparasites represent a great majority of European parasitic plants. These are root-parasitic, photosynthetic plants that germinate independently of the presence of the host and produce exclusively lateral (secondary) haustoria with a vascular connection to the host xylem only. All European species belong to the Orobanchaceae and Santalaceae. Teixeira-Costa & Davis (2021) call these plants “euphytoid parasites”, but we prefer keeping “hemiparasites” in the name of this category to preserve this well-established term.

Obligate root parasites comprise all species of non-green root holoparasites (such as Orobanche spp.), but also hemiparasitic species, which are more dependent on their host than the euphytoid hemiparasites due to the absence of photosynthesis in the initial life stage (e.g. Striga spp.). Most of them produce terminal (primary) haustoria immediately after seed germination, triggered by chemical cues of host presence. However, several European obligate root parasites (holoparasitic Lathraea spp., hemiparasitic Tozzia alpina, and perennial species of Rhynchocorys) deviate from this developmental pattern by germinating without host cues and not forming primary haustoria (Těšitel 2016).

Mistletoes are epiphytic parasitic shrubs. They germinate on host stems or branches and penetrate the host with a primary haustorium. The level of photosynthesis varies among the mistletoe species from efficient to rudimentary. The most widespread mistletoes of Loranthus and Viscum display efficient photosynthesis. By contrast, the Mediterranean genus Arceuthobium connects to the host’s phloem and takes up substantial amounts of carbon from the host (Rey et al. 1991). The photosynthetic capacity of Arceuthobium is probably limited, as shown by physiological data from their American congeners (Miller & Tocher 1975).

Parasitic vines are herbaceous parasites that attach themselves to the stems of their hosts by haustoria that are formed on the parasite stem. They germinate on the soil surface and, during a period of independent growth, forage for a host to which they attach themselves with lateral haustoria. All European parasitic vines belong to the genus Cuscuta and have only rudimentary photosynthesis, which however has an important function in seedling metabolism and seed production (McNeal et al. 2007).

Endophytic parasites (or Endoparasites) are the most integrated with the host body among parasitic plants. They are rootless, stemless and leafless, grow most of their life as filaments within their host and are only visible outside the host body when flowering. The holoparasitic Cytinus hypocistis and Pilostyles haussknechtii are the only species of this category in the European flora.

In mycoheterotrophic plants, the initial developmental stages (gametophytes in lycophytes and ferns or belowground seedling stages of other plants) are not green, obtaining all their organic carbon and other resources from the fungus. The adult stages are still dependent on the mycorrhizal fungi as a source of water and mineral nutrients but vary in their dependence on heterotrophic carbon: there is a continuum from autotrophy, where the adult plants no longer use fungal carbon (this strategy is further called ‘initial mycoheterotrophy’), through mixotrophy (the adult plants combine autotrophic with heterotrophic nutrition; further called ‘partial mycoheterotrophy’), to heterotrophy (further called ‘full mycoheterotrophy’) (Merckx 2012). Two categories are distinguished here:

Initial and partial mycoheterotrophs have been combined here into a common category because the level of carbon heterotrophy may be low or depend on light conditions (Preiss et al. 2010), which makes it difficult to distinguish between partial mycoheterotrophs and initial mycoheterotrophs. Furthermore, new partially mycoheterotrophic species may be identified due to the advancement of the stable-isotope methodology (e.g., Schiebold et al. 2018). This category includes mycoheterotrophic species from Ophioglossaceae, Lycopodiaceae, green mycoheterotrophic species from Ericaceae (subfamily Pyroloideae) and all green Orchidaceae. Species that obtain nearly all of their carbon from mycorrhizal fungi but still contain chlorophyll and can be photosynthetically active, such as Corallorhiza trifida (Zimmer et al. 2008, Cameron et al. 2009) and Limodorum species (Bellino et al. 2014) from Orchidaceae, are also included in this category. Interestingly, achlorophyllous individuals, which completely lack chlorophyll and wholly depend on their mycorrhizal fungi, are rarely found among partially mycoheterotrophic species (e.g., in the genera Cephalanthera and Epipactis).

Full mycoheterotrophs include achlorophyllous species that cannot photosynthesize and obtain carbon only from mycorrhizal fungi during their life cycle. Neottia nidus-avis and Epipogium aphyllum from Orchidaceae and Hypopitys monotropa and H. hypophegea from Ericaceae are the only species in this category in the European flora.

Categories

autotroph

euphytoid hemiparasite

obligate root parasite

mistletoe

parasitic vine

endophytic parasite

initial or partial mycoheterotroph

full mycoheterotroph

Data source and citation

Těšitel, J., Těšitelová, T., Fahs, N., Blažek, P., Knotková, K. & Axmanová, I. (2023): Parasitism and mycoheterotrophy. – www.FloraVeg.eu.

Further references

Bellino, A., Alfani, A., Selosse, M.-A., Guerrieri, R., Borghetti, M., & Baldantoni, D. (2014). Nutritional regulation in mixotrophic plants: New insights from Limodorum abortivum. Oecologia, 175(3), 875–885. https://doi.org/10.1007/s00442-014-2940-8
Cameron, D. D., Preiss, K., Gebauer, G., & Read, D. J. (2009). The chlorophyll-containing orchid Corallorhiza trifida derives little carbon through photosynthesis. New Phytologist, 183(2), 358–364. https://doi.org/10.1111/j.1469-8137.2009.02853.x
Heide-Jørgensen, H. S. (2008). Parasitic flowering plants. Brill, Leiden.
Kubat, R. & Weber, H. C. (1987). Zur Biologie von Rhynchcorys elephas (L.) Griseb. (Scrophulariaceae). Beiträge zur Biologie der Pflanzen, 62, 239–250.
McNeal, J. R., Arumugunathan, K., Kuehl, J. V., Boore, J. L., & dePamphilis, C. W. (2007). Systematics and plastid genome evolution of the cryptically photosynthetic parasitic plant genus Cuscuta (Convolvulaceae). BMC Biology, 5(1), 55. https://doi.org/10.1186/1741-7007-5-55
Merckx, V. S. F. T. (Ed). (2012). Mycoheterotrophy: the biology of plants living on fungi. Springer, Berlin.
Miller, J. R., & Tocher, R. D. (1975). Photosynthesis and respiration of Arceuthobium tsugense (Loranthaceae). American Journal of Botany, 62(7), 765–769. https://doi.org/10.2307/2442068
Preiss, K., Adam, I. K. U., & Gebauer, G. (2010). Irradiance governs exploitation of fungi: Fine-tuning of carbon gain by two partially myco-heterotrophic orchids. Proceedings of the Royal Society B: Biological Sciences, 277(1686), 1333–1336. https://doi.org/10.1098/rspb.2009.1966
Rey, L., Sadik, A., Fer, A., & Renaudin, S. (1991). Trophic relations of the dwarf mistletoe Arceuthobium oxycedri with its host Juniperus oxycedrus. Journal of Plant Physiology, 138(4), 411–416. https://doi.org/10.1016/S0176-1617(11)80515-8
Schiebold, J. M.-I., Bidartondo, M. I., Lenhard, F., Makiola, A., & Gebauer, G. (2018). Exploiting mycorrhizas in broad daylight: Partial mycoheterotrophy is a common nutritional strategy in meadow orchids. Journal of Ecology, 106(1), 168–178. https://doi.org/10.1111/1365-2745.12831
Teixeira-Costa, L., & Davis, C. C. (2021). Life history, diversity, and distribution in parasitic flowering plants. Plant Physiology, 187(1), 32–51. https://doi.org/10.1093/plphys/kiab279
Těšitel, J. (2016). Functional biology of parasitic plants: A review. Plant Ecology and Evolution, 149(1), Article 1. https://doi.org/10.5091/plecevo.2016.1097
Těšitel, J., Těšitelová, T., Blažek, P., & Lepš, J. (2016). Parasitism and mycoheterotrophy. www.pladias.cz.
Weber, H. C. (1973). Zur Biologie von Tozzia alpina L. (Standort, Wirtspflanzen, Entwicklung und Parasitismus). Beiträge zur Biologie der Pflanzen, 49, 237–249.
Zimmer, K., Meyer, C., & Gebauer, G. (2008). The ectomycorrhizal specialist orchid Corallorhiza trifida is a partial myco-heterotroph. New Phytologist, 178(2), 395–400. https://doi.org/10.1111/j.1469-8137.2007.02362.x
Carnivory: non-carnivorous

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Carnivory
Carnivorous plants attract, trap and kill their prey, mainly insects, small crustaceans and protozoans, and subsequently absorb the nutrients from the dead bodies. Carnivorous species occur in environments with extremely low availability of nutrients, especially nitrogen and phosphorus, e.g. mires. In contrast, they usually have enough light (open habitats) and high water table or precipitation levels (Fleischmann et al. 2017). Therefore, the carnivory improves the intake of nutrients essential for growth but sparse in the environment, while the main source of energy for these plants is photosynthesis (Fleischmann et al. 2017).

Although there is a variety of morphological structures and trapping mechanisms, all the traps evolved as more or less complicated modifications of leaves with glandulous hairs (Hedrich & Fukushima 2021). Examples of active-hunting carnivorous plants include Aldrovanda with snap traps and Utricularia with suction traps. Typical representatives of the passive-trapping species can be found in the genera Drosera, Drosophyllum and Pinguicula, which have specific types of adhesive leaves. Another passive mechanism is the pitfall trap of Sarracenia (Hedrich & Fukushima 2021). Some species can combine adhesive traps with active movement of either glands or parts of the leaves (e.g. some species of Drosera).

The carnivory evolved independently in relatively distant lineages of angiosperms. There are carnivorous families within the orders Poales, Oxalidales, Caryophyllales, Ericales and Lamiales (Hedrich & Fukushima 2021). This convergent evolution of carnivory was possible because the traits associated with carnivorous syndrome from trap development through prey digestion to nutrient absorption are modifications of structures found also in non-carnivorous ancestors, where these originally served as defending mechanisms (Hedrich & Fukushima 2021).

In Europe, there are only three native carnivorous families, namely Droseraceae, Drosophyllaceae (order Caryophyllales), and Lentibulariaceae (Lamiales). Carnivorous plants have however often been planted and imported to Europe. Some of these non-native carnivorous species introduced to Europe can also survive in natural habitats and establish vital populations. For example, the species of Sarracenia (Sarraceniaceae, Ericales), native to North America, have nowadays scattered secondary occurrences across western and northwestern Europe.

Categories

carnivorous

non-carnivorous

Data source and citation

Axmanová, I. (2023): Carnivory. – www.FloraVeg.eu.

Further references

Fleischmann, A., Schlauer, J., Smith, S. A., & Givnish, T. J. (2017). Evolution of carnivory in angiosperms. In Ellison, A. & Adamec, L. (Eds.), Carnivorous Plants: Physiology, ecology, and evolution (p. 22–41). Oxford University Press. https://doi.org/10.1093/oso/9780198779841.003.0003
Hedrich, R., & Fukushima, K. (2021). On the Origin of Carnivory: Molecular Physiology and Evolution of Plants on an Animal Diet. Annual Review of Plant Biology, 72(1), 133–153. https://doi.org/10.1146/annurev-arplant-080620-010429
Symbiotic nitrogen fixation: no nitrogen-fixing symbionts

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Symbiotic nitrogen fixation
Plants that are able to form a symbiosis with nitrogen-fixing bacteria are classified as nitrogen-fixing plants or nitrogen fixers. Specific bacteria are able to fix atmospheric nitrogen in a way to make it directly accessible to the plants (Franche et al. 2009). For providing nitrogen to the plant, the bacteria receive carbon in return (Crews, 1999, Dilworth et al., 2008). When forming a symbiosis with vascular plants, these bacteria usually inhabit the roots of their symbiont, forming so called (root-)nodules (Akkermans & Houwers, 1983, Fyson & Sprent, 1980, Loureiro et al., 1994). Three different symbiotic relationships between vascular plants and bacteria can be distinguished: (1) with the endosymbiotic cyanobacteria Nostoc, (2) with rhizobia (e.g. Allorhizobium, Bradyrhizobium, Mesorhizobium, Rhizobium and Sinorhizobium) and (3) with Frankia, so-called actinorhizal plants (Bond 1983, Pawlowski & Sprent 2007, Sprent 2008, Benson 2016, Tedersoo et al., 2018). Nitrogen fixation is not a completely phylogenetically conserved trait but evolved and disappeared a few times in the evolution of plants. For the first time it evolved in the Cycadales in Gymnosperms (symbiosis with cyanobacteria, plant species not native to Europe). Most of the nitrogen-fixing plants are however phylogenetically related and recruit from the so-called “Nitrogen-fixing clade” sensu Soltis et al. (1995). Only the family Zygophyllaceae (associated with rhizobia) and the non-native Gunnera, the only genus recorded in Europe associated with Nostoc, do not belong to this clade, representing the exceptions in Angiosperms. Only five native taxa (the genus Alnus, Hippophae rhamnoides, Myrica gale, Elaeagnus angustifolia and Coriaria myrtifolia) and some non-native species with sporadic occurrence are associated with Frankia in Europe. The largest number of nitrogen-fixing species form symbiosis with rhizobia. This includes almost all Fabaceae (uncertain genera and likely exceptions, respectively, are known only very few occurring in Europe: among others this includes Cercis, Erinacea, Gonocytisus, Hammatolobium, Podocytisus, Dorycnopsis (all native), Gleditsia, Cytisopsis, Styphnolobium, Gymnocladus (not native), plus Zygophyllaceae (with uncertain genera Balanites, Seetzenia and Tetraena occurring in Europe).

Assignment was done on the genus-level. Although rare cases of species-specific differences concerning the symbiotic nitrogen fixation status within one genus are known worldwide, for the European flora the general consent that the status is conserved on the genus level is still accepted. Assignment of “likely” or “unlikely” symbiosis with rhizobia is mainly based on their phylogenetic position where there has been no scientific study investigating the nitrogen fixation status of the genus directly or if studies showed diverging results.

Categories

symbiosis with rhizobia

likely symbiosis with rhizobia

unlikely symbiosis with rhizobia

symbiosis with frankia

symbiosis with cyanobacteria

no nitrogen-fixing symbionts

Data source and citation

Fahs, N., Blažek, P., Těšitel, J. & Axmanová, I. (2023). Symbiotic nitrogen fixation. – www.FloraVeg.eu.

Further references

Benson D. R. (2016). Frankia & actinorhizal plants. Available at https://frankia.mcb.uconn.edu/ [accessed on 1 Feb 2021]
Blažek, P. & Lepš, J. (2016). Symbiotic nitrogen fixation. – www.pladias.cz.
Bond, G. (1983). Taxonomy and distribution of non-legume nitrogen-fixing systems. In J. C. Gordon & C. T. Wheeler (Eds.), Biological nitrogen fixation in forest ecosystems: Foundations and applications (pp. 55–87). Springer Netherlands. https://doi.org/10.1007/978-94-009-6878-3_3
Crews, T. E. (1999). The presence of nitrogen fixing legumes in terrestrial communities: Evolutionary vs ecological considerations. Biogeochemistry, 46(1), 233–246. https://doi.org/10.1007/BF01007581
Dilworth M. J., James E. K., Sprent J. I., & Newton W. E. (Eds). (2008). Nitrogen-Fixing Leguminous Symbioses. Springer Netherlands.
Franche, C., Lindström, K., & Elmerich, C. (2009). Nitrogen-fixing bacteria associated with leguminous and non-leguminous plants. Plant and Soil, 321(1), 35–59. https://doi.org/10.1007/s11104-008-9833-8
Fyson, A., & Sprent, J. I. (1980). A Light and Scanning Electron Microscope Study of Stem Nodules in Vicia faba L. Journal of Experimental Botany, 31(123), 1101–1106.
Loureiro, M. F., DE Faria, S. M., James, E. K., Pott, A., & Franco, A. A. (1994). Nitrogen-fixing stem nodules of the Legume, Discolobium pulchellum Benth. The New Phytologist, 128(2), 283–295. https://doi.org/10.1111/j.1469-8137.1994.tb04012.x
Pawlowski, K., & Sprent, J. I. (2008). Comparison Between Actinorhizal And Legume Symbiosis. In K. Pawlowski & W. E. Newton (Eds.), Nitrogen-fixing Actinorhizal Symbioses (pp. 261–288). Springer Netherlands. https://doi.org/10.1007/978-1-4020-3547-0_10
Soltis, D. E., Soltis, P. S., Morgan, D. R., Swensen, S. M., Mullin, B. C., Dowd, J. M., & Martin, P. G. (1995). Chloroplast gene sequence data suggest a single origin of the predisposition for symbiotic nitrogen fixation in angiosperms. Proceedings of the National Academy of Sciences of the United States of America, 92(7), 2647–2651.
Sprent, J. I. (2008). Evolution and Diversity of Legume Symbiosis. In M. J. Dilworth, E. K. James, J. I. Sprent, & W. E. Newton (Eds.), Nitrogen-fixing Leguminous Symbioses (pp. 1–21). Springer Netherlands. https://doi.org/10.1007/978-1-4020-3548-7_1
Tedersoo, L., Laanisto, L., Rahimlou, S., Toussaint, A., Hallikma, T., & Pärtel, M. (2018). Global database of plants with root-symbiotic nitrogen fixation: NodDB. Journal of Vegetation Science, 29(3), 560–568. https://doi.org/10.1111/jvs.12627

Habitat and sociology

Syntaxon

Diagnostic species of phytosociological classes: GC (LAU) Pruno lusitanicae-Lauretea azoricae, GD (AZO) Lauro azoricae-Juniperetea brevifoliae

EUNIS habitat

Diagnostic species of EUNIS habitats: S43 Macaronesian heath

Constant species of EUNIS habitats: S43 Macaronesian heath

Broad habitat

Occurrence in broad habitats: Heathland, Forest

Distribution

Country-based map: Euro+Med Plantbase

No subordinate taxa were found for this item.