Amaranthus Tuberculatus (Moq.) J.D
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BioInvasions Records (2020) Volume 9, Issue 3: 642–654 CORRECTED PROOF Research Article Amaranthus tuberculatus (Moq.) J.D. Sauer – a new alien pigweed species in Croatia Anja Rimac*, Marko Doboš and Vedran Šegota Division of Botany, Department of Biology, Faculty of Science, University of Zagreb, Marulićev trg 20/II, 10000 Zagreb, Croatia Author e-mails: [email protected] (AR), [email protected] (MD), [email protected] (VŠ) *Corresponding author Citation: Rimac A, Doboš M, Šegota V (2020) Amaranthus tuberculatus (Moq.) Abstract J.D. Sauer – a new alien pigweed species in Croatia. BioInvasions Records 9(3): Amaranthus tuberculatus, commonly known as the rough-fruited water-hemp, is a 642–654, https://doi.org/10.3391/bir.2020.9.3.19 dioecious annual weed species originating from North America. It has been introduced into Europe and Asia, where it is mostly considered a naturalized or Received: 22 January 2020 casual alien occupying riparian areas, agricultural fields and disturbed habitats, Accepted: 14 April 2020 especially in commercial port areas. Here we report the first occurrence of the Published: 12 June 2020 species in Croatia, the second in Southeastern Europe. Flowering male and female Handling editor: Quentin Groom individuals were found in 19 localities in the Pannonian part of Croatia. Female Thematic editor: Stelios Katsanevakis individuals from all localities had flowers with only one tepal and a dehiscent fruit Copyright: © Rimac et al. and were therefore identified as A. tuberculatus var. rudis. In the studied area, the This is an open access article distributed under terms species was most frequently recorded along the banks of the Sava River and of the Creative Commons Attribution License eutrophicated drainage channels passing through arable land. Here, it was present (Attribution 4.0 International - CC BY 4.0). within vegetation of the alliance Nanocyperion Koch 1926 (class Isoëto-Nanojuncetea OPEN ACCESS. Br.-Bl. et Tx. in Br.-Bl. et al. 1952) and the alliance Bidention tripartitae (class Bidentetea Tx. et al. ex von Rochow 1951), as well as on the edges of alluvial willow and poplar forests (Salicion albae Soó 1951, class Salicetea purpureae Moor 1951). Furthermore, it was recorded on river sandbars, concrete embankments and other disturbed habitats (along the railroad, a road, on a construction site). Although the species is a well known agricultural weed and the majority of our study area is composed of arable land, A. tuberculatus was not detected in this habitat type. However, we believe that it is highly probable that it will spread into new areas and suitable habitats, and strongly recommend the occupied area to be monitored. Key words: alien plant species, amaranth, Amaranthus rudis, Balkan Peninsula, riparian habitats, Sava River, Southeastern Europe, weed Introduction Amaranthus L., also known as amaranth or pigweed, is a genus of worldwide distribution, including about 70–75 species, the majority of them being native to the Americas (Costea et al. 2001; Mosyakin and Robertson 2003; Iamonico 2015a). The genus is economically important since some of its representatives are useful cultivated plants, such as grain amaranths, leaf vegetables, fodder plants, potherbs and ornamentals (Sauer 1967). On the other hand, some are noxious and widespread agricultural weeds that outcompete cultivated plants and have a detrimental impact on agriculture (Weaver and McWilliams 1980; Holm et al. 1991; Costea and Tardif 2003b; Costea et al. 2004). This explains why so many species of the Rimac et al. (2020), BioInvasions Records 9(3): 642–654, https://doi.org/10.3391/bir.2020.9.3.19 642 Amaranthus tuberculatus in Croatia genus are already naturalized or are reported as casual aliens outside their natural range. In Europe, for instance, there are only three indigenous Amaranthus species, while as many as 40 species are reported as introduced, either adventive or naturalized (Iamonico 2015b). There are 13 species of the genus Amaranthus reported so far from Croatia, with only one species – A. blitum, recognized as native, while the rest are introduced, mostly originating from North America. Furthermore, five of them are listed as invasive (Nikolić 2019). Here we present and discuss a new addition to the alien flora of Croatia and Southeastern Europe, Amaranthus tuberculatus (Moq.) J.D. Sauer, commonly known as a rough-fruited water-hemp, its currently known distribution in the country, as well as the habitats and vegetation types occupied. Amaranthus tuberculatus is a dioecious, annual herb originating from North America. A detailed description of morphology can be found in Mosyakin and Robertson (2003), Costea et al. (2005) and Iamonico (2015c). Taxonomical difficulties have given rise to numerous synonyms, one of them being Amaranthus rudis J.D. Sauer (Costea et al. 2005; The Plant List 2019). Sauer (1955) recognized two water-hemp species – A. tuberculatus and A. rudis, which are morphologically distinguished by indehiscent fruit and absence of tepals in pistillate flowers in A. tuberculatus and the dehiscent fruit and one or two, lanceolate or linear tepals in pistillate flowers in A. rudis. Later on, Pratt and Clark (2001) included A. rudis in the synonymy of A. tuberculatus, recognizing a single polymorphic species, with inconsistent morphological characteristics representing a single species continuum. On the other hand, Costea and Tardif (2003a), proposed their recognition at the varietal level – A. tuberculatus var. tuberculatus and Amaranthus tuberculatus var. rudis (J.D. Sauer) Costea & Tardif. While its native range is still under debate (Iamonico 2015a), the species is nowadays widespread across both the USA and Canada, being a major weed of agricultural fields and other disturbed habitats far outside its original range. Amaranthus tuberculatus was introduced into Europe and Asia in the 20th century. It has been reported from 15 European countries so far, mostly as an ephemeral species (Iamonico 2015b). According to the available literature, it was first recorded in Austria in the 1940s (Aellen 1959; Essl and Rabitsch 2002; NOBANIS 2019) and has also been introduced into Belgium (Verloove and Vandenberghe 1993; Verloove 2006), the Czech Republic (Pyšek et al. 2002), Denmark, Finland (Jonsell 2001), Germany (Schmitz 2002; Buttler and Thieme 2018), Great Britain (Brenan 1961), Italy (Soldano 1982; Celesti-Grapow et al. 2010), Netherlands (Van der Meijden et al. 2003), Romania (Anastasiu and Negrean 2006), Russia (Tzvelev 2012), Slovenia (Čep 2014; Lešnik 2017), Spain (Sánchez Gullón and Verloove 2013), Sweden (Iamonico 2015a) and Ukraine (Mosyakin 1995, 1996). In Asia, the species was first recorded in Israel in 1970 Rimac et al. (2020), BioInvasions Records 9(3): 642–654, https://doi.org/10.3391/bir.2020.9.3.19 643 Amaranthus tuberculatus in Croatia (Greuter and Raus 1986; Danin and Fragman-Sapir 2019), followed by Jordan (Di Castri et al. 1990) and Japan (Mito and Uesugi 2004). In its native and introduced range, the species primarily occurs on the margins of freshwater (rivers, lakes and ponds) and in wetlands. Furthermore, it successfully grows in disturbed habitats, such as roadsides, railroads and wasteland or as a weed in cultivated fields and gardens (Pratt and Clark 2001; Mosyakin and Robertson 2003; Costea et al. 2005; Iamonico 2015c). Outside its native range, A. tuberculatus is mostly recognized as an ephemeral or naturalized alien (Iamonico 2015b). It exhibits high phenotypic plasticity and genetic variability, which, along with a high level of interspecific hybridization and introgression, could enable rapid adaptation to newly invaded areas (Costea et al. 2005). Furthermore, the species exhibits a high growth rate, the production of a large number of viable and easily dispersed seeds and develops a persistent seed bank, all of which contributes to the rapid progress of the species after its initial establishment, provided that both male and female individuals were introduced at the same time (Costea et al. 2005). Materials and methods Study area The fieldwork was performed in the summer of 2019 in the Pannonian part of Croatia, as a part of two independent projects. One project focused on the monitoring of aquatic and riparian vegetation of the watercourses, covering the majority of the Pannonian part of Croatia, while the aim of the other project was the mapping of invasive alien plant species, in a more restricted area of Brodsko-Posavska and Požeško-Slavonska counties. The latter covered ruderal habitats, urban areas and disturbed habitats in general, as well as riparian habitats, where the occurrence of alien species could be expected. All our localities are situated in the catchment area of the Sava River, a large lowland river, belonging to the Black Sea Basin. The Sava River rises in the Triglav group of the Julian Alps, flows mainly east-southeastward through Slovenia and Croatia, where it forms the border between Croatia and Bosnia and Herzegovina, before entering Serbia and joining the Danube River at Belgrade, after a course of about 940 km. The Sava River is navigable downstream from Sisak, with one of the ports in Slavonski Brod, a major urban area of the Pannonian part of Croatia. Most of the studied area is still rural, with arable land dominating the landscape. Sampling and identification At each locality, individuals were collected for later identification, dried and deposited in the herbarium collection ZA (Thiers 2019). The specimens were identified using several identification keys (Costea and Rimac et al. (2020), BioInvasions Records 9(3): 642–654, https://doi.org/10.3391/bir.2020.9.3.19 644 Amaranthus tuberculatus in Croatia Figure 1. Study area and localities of Amaranthus tuberculatus in Croatia. For the description of the locality number, see Table 1. Tardif 2003a; Mosyakin and Robertson 2003; Costea et al. 2005; Bayón 2015; Iamonico 2015c) and photographed in the field and the laboratory under stereomicroscope. Furthermore, vegetation types and plant species at each locality were listed, as well as habitat types occupied by Amaranthus tuberculatus.