Review Article |
Corresponding author: Ivan Hoste ( ivan.hoste@plantentuinmeise.be ) Academic editor: Marcin Nobis
© 2022 Ivan Hoste, Filip Verloove.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Hoste I, Verloove F (2022) Taxonomy of the weed species of the genus Echinochloa (Poaceae, Paniceae) in Southwestern Europe: Exploring the confused current state of affairs. PhytoKeys 197: 1-31. https://doi.org/10.3897/phytokeys.197.79499
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The taxonomy of Echinochloa, a predominantly tropical to warm-temperate genus of 40–50 species, including some of the world’s worst weeds, is still poorly understood. This is because some species, including the extremely widespread E. crus-galli, show a wide range of morphological, physiological and ecological variation, in part the result of a complex recent evolutionary history. Furthermore, there is often a dearth of clear distinguishing features among species. The same applies to the species established in Southwestern Europe, where unintentionally introduced populations have now established themselves as important weeds of crops, especially maize and rice. Taxonomic and nomenclatural confusion hampers progress in weed science. In this study, we give an identification key that covers the weedy taxa encountered in Southwestern Europe, followed by notes on taxonomy and nomenclature. Moreover, a lectotype is designated for Echinochloa frumentacea. It is argued that current confusion cannot be overcome without including populations of Eastern Asian origin in taxonomic studies and without the joint efforts of experts in the fields of weed science, morphology-based taxonomy, genomics and phylogenetics.
Echinochloa, evolutionary history, lectotypification, nomenclature, Poaceae, Southwestern Europe, taxonomy
Echinochloa P. Beauv. is a predominantly tropical to warm-temperate genus of 40–50 species that are usually associated with wet or damp places (
The taxonomy of Echinochloa is still poorly understood, resulting in strongly diverging interpretations of its classification and nomenclature. These divergent interpretations can be attributed to several reasons, such as the wide range of within-species variation (not in the least in ill-defined and polymorphic E. crus-galli), the recurrent absence of unequivocal qualitative and quantitative distinguishing features among species, insufficient joint research by taxonomists and agronomists and the often extended lag time between the introduction of an exotic taxon in a new geographic region and its detection and correct identification by local botanists and weed scientists. As a result of the description of numerous taxa with probably little or no taxonomic value, quite a few species may be overvalued.
In Southwestern Europe, taxonomically widely divergent treatments of the genus Echinochloa are available for the British Isles (
In an overview of the weedy species of Echinochloa in Southwestern Europe,
Distinguishing between American E. muricata and European E. crus-galli based on morphology is relatively easy, yet separating the latter from persistent and morphologically variable Echinochloa introduced from Asia and today thriving in rice fields in Southern Europe proves much more difficult. The contrasting treatments of Echinochloa in Japanese (
To develop superior control methods in crops, including rice and maize, basic knowledge of the classification, morphology, physiology and ecology of specific weeds is essential (
Morphology-based distinguishing traits frequently used in keys and descriptions often find no confirmation in molecular data. An attempt to bridge the gap with a modified “simple and effective morphological key” (
Identification keys for Echinochloa in floras or weed science papers are often restricted to a rather small geographical area. Covering a larger area and more taxa may lead to more attention being paid to taxa which, so far, could have been overlooked. As far as the reviewed European literature is concerned, this paper is mainly restricted to Southwestern Europe, roughly stretching from the British Isles in the north to the Iberian Peninsula and Italy in the south. The key should, however, prove useful to identify the established weedy species of the genus Echinochloa in most of Europe. Owing to nomenclatural and taxonomic uncertainties, the key is considered provisional; for a different recent interpretation, see
A number of rare casuals that have been reported from Europe in the past, for instance, as wool aliens, have been omitted. These include Echinochloa inundata Michael & Vickery and E. jubata Stapf from Belgium (
Echinochloa crus-pavonis has been excluded from the key since the records from rice fields in Southern Europe seem to be based on erroneous identifications (
Those who run into problems when using the key given below or suspect they are dealing with a species missing from the key are referred to the keys to the annual and perennial species of Echinochloa produced by P.W.
In combination with the wide variation within individual species, the dearth of strong qualitative and quantitative features precludes easy identification in the genus Echinochloa. Within the same inflorescence, the spikelets may show considerable variation. The number, size, position and direction of hairs and bristles is often strongly influenced by competition for space among the closely packed spikelets. The length of the lower glume and the shape of the sterile lemma (occasionally part of them shiny and convex) can be assessed only by examining several spikelets. The length of the spikelet – excluding the awn of the sterile lemma – is an important feature (
1 | Fertile floret not disarticulating at maturity. Spikelets unawned. Fertile floret and caryopsis markedly humped. Inflorescence compact, usually contracted and with the axis often hardly visible, sometimes with spreading branches (Fig. |
2 |
1' | Fertile floret disarticulating at maturity. Spikelets awned or not. Fertile floret and caryopsis not markedly humped. Inflorescence not strongly contracted when fully developed, with the axis showing through (but compare with clearly different E. muricata var. wiegandii when in doubt) | 3 |
2 | Spikelets dark brownish or purplish at maturity (Fig. |
E. esculenta |
2' | Spikelets pale (yellowish or greenish) at maturity (Fig. |
E. frumentacea |
3 | Spikelets < 3 mm long and lower glume ca. 1/2 length of the spikelet, which is always unawned. Axis of the inflorescence branches (almost) without bristles (except at the base). Inflorescence without secondary branches (Fig. |
E. colona |
3' | Spikelets usually ≥ 3 mm long, awned or not. (If spikelet < 3 mm, then lower glume only ca. 1/3 length of the spikelet.) Axis of the inflorescence branches with bristles. Inflorescence often with secondary branches. Leaves usually wider. Caryopsis usually darker, yellowish or brownish | 4 |
4 | Spikelets ≥ 4 mm long and at least some spikelets with lower glume up to 2/3 length of the spikelet (Fig. |
E. oryzicola |
4' | Spikelets ≥ 4 mm long and lower glume not longer than 1/2 length of the spikelet. Mature inflorescence drooping (Fig. |
E. crus-galli var. oryzoides |
4" | Spikelets ≤ 4 mm long and lower glume usually clearly less than 1/2 length of the spikelet. (If spikelets > 4 mm, see 6, E. muricata var. muricata. Solely a rare casual?) | 5 |
5 | Lemma of the fertile floret with a membranous tip that is clearly differentiated from the coriaceous body of the lemma (Fig. |
E. crus-galli |
5' | Lemma of the fertile floret with a stiff, smooth tip, not clearly differentiated from the coriaceous body of the lemma (Fig. |
6 |
6 | Spikelets ≤ 3.5 mm long, with strongly spreading papilla-based bristles (which give the spikelet a rugged appearance), unawned or at most with an elongated tip (Fig. |
E. muricata var. microstachya |
6' | Spikelets ≤ 3.5 mm long; the papilla-based bristles not strongly spreading. Numerous spikelets in the inflorescence with a short awn (sometimes up to ca. 10 mm) (Fig. |
var. wiegandii |
6" | Spikelets ≥ 3.5 mm long; numerous spikelets in the inflorescence with a longer awn (up to 16 mm). (Apart from the presence of awns, the rugged spikelets look like a more robust version of var. microstachya.) (Probably only a rare casual.) | var. muricata |
Panicum colonum L., Syst. Nat. (ed. 10) 2: 870. 1759.
LINN-80.23 (lectotype, designated by
Echinochloa colona is usually easy to identify, yet care should be taken to distinguish it from forms with small spikelets of E. crus-galli (
Panicum crus-galli L., Sp. Pl. 1: 56. 1753.
Herb. Burser 1: 303, sine dato (UPS).
There has always been a great deal of confusion about the type; see, e.g.,
=Echinochloa crus-galli subsp. spiralis (Vasinger) Tzvelev, Zlaki SSSR 662. 1976. Basionym: Echinochloa spiralis Vasinger, Flora SSSR 2: 739–740. 1934. Type: Caucasus: Kuban: Krasnodar vic., 28 Oct 1931, A.V. Vazinger-Alektorova s.n. (holotype; LE).
=Echinochloa crus-galli var. praticola Ohwi, Acta Phytotax. Geobot. 11: 37 1942. Type: Kiushiu, m. Kujusan, U. Faurie 2646 (holotype; KYO). Image available at http://www.museum.kyoto-u.ac.jp/collection/PlePlant/PlePlant00001775_1.htm.
= Echinochloa crus-galli var. hispidula (Retz.) Honda, Bot. Mag. (Tokyo) 37: 122. 1923.Basionym:Panicum hispidulum Retz., Observ. Bot. 5: 18. 1789. Type: India: “India orientali”, without data, König s.n. (LD 1219266) (lectotype, designated by
= Echinochloa erecta (Pollacci) Pignatti, Arch. Bot. 15(1): 2. 1955. Basionym:Panicum erectum Pollacci, Atti Ist. Bot. Univ. Pavia 13: 228, t. 5. 1908. Type:
Italy: Lombardia, Presso Pavia, Oct 1907, G. Pollacci s.n. (lectotype, designated by
Panicum oryzoides Ard., Animadv. Bot. Spec. Alt. 2: 16, pl. 5. 1764.
LINN 80.68. Image available at https://linnean-online.org/1302/.
According to
Echinochloa crus-galli s.l. is taxonomically the most complex Echinochloa occurring as a weed in Southwestern Europe. As we understand, this species occurs in a number of varieties, but E. oryzicola is not one of them and is accepted as a separate species (see below). As a result of a long and complex evolutionary history, including significant modifications in the recent past (after the introduction of agriculture), the differences among the varieties are often slight. Furthermore, introductions of several taxa as weeds in a range of crops far outside their natural range have contributed to obscuring their original geographical distribution. Rather than aiming at precisely describing the limits and defining features of varieties of E. crus-galli occurring in Southwestern Europe, we restrict ourselves primarily to indicating where unsolved problems remain.
Being extremely polymorphic, numerous varieties of E. crus-galli have been described, many of them based on the presence or absence of awns. As the development of awns is influenced by environmental conditions (
There is a broad consensus that E. crus-galli var. crus-galli occurs in large parts of Europe and Asia, but authors differ on how to appropriately define it.
According to
Spikelets of Echinochloa oryzicola A fertile lemma with the tip differentiated from the coriaceous body of the lemma (upper glume removed) B, C two spikelets with convex shiny sterile lemma D spikelet with long lower glume and non-shiny sterile lemma. (Photograph: André De Kesel, Meise Botanic Garden).
Within E. crus-galli as interpreted here, var. oryzoides is the most easily identified variety, clearly distinguished by the large size of its spikelets. Although the descriptions given in triplet 4 in the key above may suggest otherwise, it is not always easy to distinguish between var. oryzoides and E. oryzicola; see the discussion about the latter species below. At one time, the name Echinochloa hostii (M. Bieb.) Link was used by Italian botanists (
Recently,
Among the forms with small spikelets, subsp. spiralis (Vasinger) Tzvelev (no combination available as a variety) and var. praticola Ohwi have been mentioned as occurring in Europe. Apparently solely based on the small spikelets, both names were synonymised by
A rather distinct form of E. crus-galli with spikelets ca. 3 mm long or a little longer (somewhat smaller than average var. crus-galli) has occasionally been observed in Belgium, including in the border of maize fields where, however, it seems not to establish easily and disappears after only a few years. These plants usually have an erect habit and rather stiff leaves. The inflorescence is erect, with patent branches. The purple-tinged spikelets are usually unawned (but a few spikelets may have a long awn), and some have a glabrous, convex and shiny sterile lemma. The lower leave sheaths vary from glabrous to densely covered with short retrorse hairs.
Considering the preceding discussion, we accept, for the present, only few varieties of E. crus-galli as occurring in Southwestern Europe. Indigenous and quite variable var. crus-galli, usually with a less erect habit and more floppy leaves, is by far the most widespread variety, especially towards the north. Part of the variation observed in Europe is perhaps due to the involuntary introduction and establishment of populations of var. crus-galli, with slightly different morphological features, from Asia. Echinochloa crus-galli var. oryzoides, characterised by large spikelets, a more erect habit and stiffer leaves, is a rice mimic in rice fields of Southern Europe. Echinochloa crus-galli var. hispidula , in some respects resembling var. crus-galli and in others var. oryzoides , appears to us not to deserve a separate status and is, therefore, included in var. crus-galli.
Plants with small spikelets are the most difficult to interpret. Probably representing more than one taxon – quite possibly including taxonomically irrelevant forms of var. crus-galli – they require additional study, which will need to include material of Asian origin.
Finally, it can be argued that Echinochloa esculenta (A. Braun) H. Scholz, a cultivated taxon derived from E. crus-galli, should be included in E. crus-galli (
Panicum esculentum A. Braun, Index Sem. [Berlin] 1861(App.): 3. 1861.
Koernicke s.n., Cult. Hort. Bonn-Poppelsdorf, 28 Oct 1875 (B) (neotype, designated by
See the combined comments below, under E. frumentacea.
India, Roxburgh s.n. (K000215131, the specimen on the extreme right on the sheet). Image available at http://specimens.kew.org/herbarium/K000215131.
The protologue refers to a Roxburgh collection from India (“Roxb. ind. 1. 307. R. S. m. 2. 250. Hab. in India orientali ubi colitur”). The Kew herbarium houses two original but undated Roxburgh collections (sheets K000215131 and K000215132) that can serve for a proper typification. None exactly matches the information provided in the protologue, but since Link described the species in 1827, i.e. well after Roxburgh’s (1751–1815) death, these collections are supposed to have been at his disposal when describing the species. In the apparent absence of other original material, one of the two above-mentioned Kew collections could be chosen as the lectotype for that name. Digital images of both are easily accessible via online resources such as the Kew Herbarium Catalogue, JSTOR or POWO. Sheet K000215131 comprises five stems, four of which have an inflorescence. The extreme left specimen is atypical and might as well represent a different species. The other flowering specimens are representative for the species, and the specimen on the extreme right is here designated as the lectotype for the name E. frumentacea. According to
Echinochloa esculenta (syn.: E. utilis Ohwi & Yabuno) and E. frumentacea are cultivated species. Neither is considered a persistent weed in Southwestern Europe. Still, they are included in the key since they are the most frequently occurring non-weedy representatives of the genus in Southwestern Europe, frequently recorded as bird-seed aliens in and along the border of crop fields (
Habit of Echinochloa crus-galli var. crus-galli growing as a roadside weed, Belgium. Although extremely variable, the usually more or less procumbent habit (the lower nodes often rooting) and the floppy leaves are among the features that distinguish var. crus-galli from the obligate rice weeds E. crus-galli var. oryzoides and E. oryzicola which are characterised by a more erect and stiffer habit. (Photograph: Luc Audenaerde).
Setaria muricata P. Beauv., Essai Agrostogr. 51, 170, 178. 1812.
Canada: Quebec Lac Champlain, s.d., A. Michaux s.n. (holotype: P-MICHX, isotype: US-80768).
USA: New York, Tompkins Co., Ithaca, between Fall Creek, Inlet and city, waste soil, border of west marsh, open alluvial and marshy flats, 19 Jul 1913, E.L. Palmer 097 (GH). Image available at https://s3.amazonaws.com/huhwebimages/755E8AFFFFF6435/type/full/303931.jpg.
Echinochloa pungens var. wiegandii Fassett, Rhodora 51(601): 2. 1949.
USA: Oregon, Hayden Island, sandy roadside, J.C. Nelson 1974, 8 Sep 1915 (holotype GH). Image available at https://kiki.huh.harvard.edu/databases/specimen_search.php?mode=details&id=126740.
Echinochloa muricata is native to North America. Its status as separate from E. crus-galli, which was inadvertently introduced there long ago from Europe, was contested by
Echinochloa muricata is a highly variable species, though less so than E. crus-galli. This, combined with its resemblance to E. crus-galli, has added to the difficulty for agronomists and botanists on both sides of the Atlantic to detect and correctly name its introduced populations. Early records of introduced E. muricata from France revealed morphologically very uniform populations (as E. pungens [Poir.] Rydb. var. microstachya [Wiegand] Fernald & Griscom;
The European populations of E. muricata exhibit only part of the variation found in the natural range of the species. So far, three morphologically distinct varieties have been recorded from Belgium and France. Echinochloa muricata var. muricata, with larger spikelets, seems to occur only as an ephemeral alien (
Echinochloa muricata is a species of moist, disturbed sites. It is not an important weed of rice fields (
=Echinochloa phyllopogon auct., non (Stapf) Stapf ex Kossenko in Botanicheskie Materialy Gerbariia Botanicheskogo Instituta imeni V. L. Komarova Akademii Nauk SSSR 8(12): 208. 1940.
=E. hostii auct. ital., non (M. Bieb.) Link, Hort. Berol. 2: 209. 1833.
Panicum oryzicola Vasinger, Trudy Prikl. Bot. 25(4): 125. 1931.
Vladivostok region, left bank of Santakheza, 4 km east of Lake Hanka, 23 Aug 1928, A. Venzinger-Alexandrova (lectotype, designated by
Although sometimes included in E. crus-galli, several features justify accepting E. oryzicola as a separate species. Echinochloa oryzicola is tetraploid (2n = 36), whereas E. crus-galli is hexaploid (2n = 54) (
The treatment of the rice mimics E. oryzicola and E. crus-galli var. oryzoides in taxonomic and agronomic publications has been extremely confusing. In the past, the name E. phyllopogon, often without author citation and thereby adding to confusion, was used separately for each of the two taxa as well as for both of them together; see, e.g., the shifting interpretation in successive publications by
Schematic reconstruction of the evolutionary history of Echinochloa oryzicola, E. crus-galli and two rice mimics derived thereof. It is hypothesised that the taxon that today is called E. oryzicola has only recently evolved from a wild taxon that seems no longer to exist or has not yet been identified. In the absence of information on this original species, it is impossible to distinguish between a long-existing taxon (‘var. oryzicola’) and a recently evolved rice mimic (‘var. infestans’).
The separate status of E. oryzicola has been corroborated by molecular studies (e.g.,
Unfortunately, the structure of the tip of the fertile lemma, which clearly distinguishes E. crus-galli from E. muricata (
Defined as “an ubiquitous plant, with variation you can’t get your teeth into, which clutters up herbaria” (
So far, Echinochloa has not benefitted from the recent revival of interest in botanical monographs, which has primarily been kindled by biodiversity and conservation concerns, especially in the species-rich tropics, rather than by hopes of improving the means to control economically damaging weeds (
The expression ‘evolutionary history’ here refers to more than ‘ancestry of a species’ as routinely used by biologists when describing ‘natural’ events. It also involves human history and the role humans have played, consciously or not, in the origin and evolution of plant species (
Echinochloa muricata exhibits a high degree of variation. Although within North America the distribution of the different forms has been altered as the result of human activities, such as land reclamation (
Circa 10 millennia ago, Echinochloa spp., along with other wetland grasses such as rice (Oryza spp.), was gathered and processed for human consumption in China (
Echinochloa crus-galli is usually autogamous. When unconsciously transported around the world with rice seed, the introduction of morphologically different forms may, therefore, result in the establishment of seemingly quite distinct taxa (
From this short detour into the evolutionary history of Echinochloa in Southeast Asia, one can conclude only that the study of the taxonomy of this genus in Europe requires a broader geographical scope. This should be coupled with the consideration of some questions that so far have been insufficiently addressed. The morphological and genetic variation of E. crus-galli var. crus-galli within its extensive Old World native range is poorly documented, as are the interactions (occasional cross-pollination of usually autogamous plants) between populations of var. crus-galli and those of the derived rice mimics. As for E. oryzicola, in the absence of information about its non-mimic ancestor, its evolutionary history is quite obscure. Identifying the unknown diploid parent species that, together with tetraploid E. oryzicola, gave rise to E. crus-galli would help better understand the species complex of E. crus-galli and E. oryzicola, including ‘E. glabrescens’.
Embedding these questions in a larger project of a world monograph of Echinochloa, the outcome of the collaboration of experts in the fields of taxonomy, genomics and phylogenetics, would enhance our understanding of the affinities between weedy and non-weedy taxa, and between Old and New World species. Moreover, such a project could generate a great deal of knowledge about the evolutionary history of a group of plants that has undergone profound changes resulting from its interactions with humans in the course of the past millennia.
We thank Benny De Cauwer (Ghent University) for sharing unpublished data on E. muricata with us, and Manuel-Benito Crespo Villalba (Depto. Ciencias Ambientales y Recursos Naturales [Botánica] Universidad de Alicante) for making available the not yet published manuscript on Echinochloa for Flora Iberica and his comments on the early versions of the Ms. Illustrations 1–4, 9 and 12 courtesy Waarnemingen.be, Stichting Observation International and the local partners. Alexander Sukhorukov (Moscow State University) provided information on relevant Russian literature.