6.5 (Peakall and Smouse, 2012). doi: 10.2307/3298527. The gene diversity (h), allelic richness (AR), and coefficient of inbreeding (FIS), and its confidence intervals were calculated using FSTAT ver. 35 (4), 444.452. doi: 10.1016/j.ecoleng.2008.05.020, Wang, X. Y., Shen, D. W., Jiao, J., Xu, N. N., Yu, S., Zhou, X. F., et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). A global assessment of invasive plant impacts on resident species, communities and ecosystems: the interaction of impact measures, invading species’ traits and environment. Sci. 101 (38), 13804–13807. Bioinformatics 28 (19), 2537–2539. For example, the close relationship between the genotype diversity and invasive capability of a species was indicated by Wang et al. We sampled vegetative and reproductive traits in the field at 20 sites over 20° latitude in China (invasive range) and 28 sites over 17° in the US (native range). Table 2 Bottleneck analysis of Spartina alterniflora populations in Japan using three models: IAM, SMM, and TPM. Reconstructing a century of Spartina alterniflora invasion with historical records and contemporary remote sensing. Seed germination characteristics of invasive Spartina alterniflora Loisel in Japan: implications for its effective management. (2009). Chung, C. H. (1989). Eng. Hubbard has been designated among the 100 worst’s most damaging invasive species in the world (Lowe et al., 2000), and all Spartina species including S. alterniflora have been declared “designated invasive alien species” on the Act on the Prevention of Adverse Ecological Impacts Caused by Designated Invasive Alien Species of Japan in 2014 (Ministry of the Environment, … (2007), who indicated that samples should be collected from colonies that are at least about 2.5 m apart from each other (Supplementary Table 1). A TaKaRa PCR Thermal Cycler (TaKaRa BIO, Shiga, Japan) was used for the PCR assay. (2001). Coastal wetlands in mainland China are critically important to shorebirds. Weed Res. Plant Sci. This fact suggests that S. alterniflora populations in the Willapa Bay might be derived from multiple populations on the Atlantic coast around New York (i.e., mid-Atlantic source) (Blum et al., 2007). Posted on December 15, 2020 Categories: All News. (2012). The value of g indicates the rate of the individuals with duplicate clones removed in each local population. doi: 10.1046/j.1365-294x.2000.00876.x, PubMed Abstract | CrossRef Full Text | Google Scholar, An, S. Q., Gu, B. H., Zhou, C. F., Wang, Z. S., Deng, Z. F., Zhi, Y. All names of the haplotypes obtained in this study were assigned according to the method of Blum et al. (2005) indicated that multiple introductions of invasive populations appear to be the rule rather than the exception, while other researchers have reported that the frequency of introductions may greatly contribute to the decrease of genetic diversity in these populations if a highly competitive species has invaded a region rich in genetic diversity, and to the relief from inbreeding depression over the short run (years to decades) (e.g., Frankham et al., 2002; Saltonstall, 2002; Dlugosch and Parker, 2008). To compare the chloroplast DNA (cpDNA) haplotypes of S. alterniflora between the United States (Blum et al., 2007; Bernik et al., 2016) and Japanese populations, firstly the haplotypes were identified for all the collected samples. 90 (4), 502–503. Thus, to validate this hypothesis, trade histories were compared between countries/regions where S. alterniflora has grown (the United States, China, Taiwan, Hong Kong) (Blum et al., 2007; Guo et al., 2015; Bernik et al., 2016) and the ports nearest to each studied river in Japan (i.e., Kumamoto Port, Yatsushiro Port, and Mikawa Port) using historical trade data from the 2003 to 2013 in the Global Trade Atlas (https://www.gtis.com/gta/). Populations of S. alterniflora in the Grays Harbor, Washington (haplotype B) and Taiwan (haplotype C4), which had only a single haplotype as well as Japan (Figure 2), were unintentionally and secondarily introduced from the Willapa Bay, Washington (the Pacific coast of the U.S.) (Civille et al., 2005) and the vicinity of Fujian (China) (Lin et al., 2015), respectively. Ecol. International trade serves as one of the driving factors for the widespread invasion of the invasive species (Elton, 1958; Lockwood et al., 2007; Davis, 2009; Richardson, 2011). (Poaceae) Introduced Unintentionally Into Japan and Its Invasion Pathway. Ecol. It is suggested that although these individuals have actually grown via seed propagation (i.e., sexual reproduction), they may be considered as clones with exactly the same genotype due to the extreme homozygosity. In a laboratory incubation experiment lasting for 153 days, we used two types of soil which were collected from invasive S. alterniflora and native Phragmites australis marshlands, and traced the transformation of 13 C from leaf and root litter of invasive Spartina alterniflora into CO 2, soil-dissolved organic C (DOC), microbial biomass C (MBC), and soil organic C (SOC). In Aichi Prefecture, 27 samples (i.e., one individual per colony) were collected from multiple colonies along and around the Umeda River (N34° 42′, E 137° 18′) facing the Mikawa Bay. Preliminary studies of introduced Spartina alterniflora Loisel in China (I). ★ indicates the region estimated as the place that S. alterniflora was initially introduced into China, according to Bernik et al. We would like to thank Dr. Tadao Kitagawa, Dr. Takuo Sawahata, Dr. Kaori Kochi, Takahiro Kusaka (Kindai University), Kano Koide (Japan Wildlife Research Center), and Reiko Ito (Kyushu Kaihatsu Engineering Co., Ltd.) for their helpful suggestions and supports regarding this manuscript. (2009). doi: 10.1002/ecy.2863, Bossdorf, O., Auge, H., Lafuma, L., Rogers, W. E., Siemann, E., Prati, D. (2005). species are known to have been deliberately introduced into the bay in the 1970's as part of marsh restoration projects. Rep. 10, 2116. doi: 10.1038/s41598-020-58879-7, Hoos, P. M., Miller, A. W., Ruiz, G. M., Vrijenhoek, R. C., Geller, J. Nucleic Acids Res. Eng. Xu, G. W., Zhou, R. Z. doi: 10.2307/2403612. Hortus Northwest 6, 9–12, 38-40. Search for more papers by this author . How to report an invasive species sighting to EDDMapS – Early Detection & Distribution Mapping System. Microsatellite analysis was conducted using 11 microsatellite markers (SPR1, SPR2, SPR3, SPR4, SPR5, SPR6, SPR7, SPR8, SPR9, SPR10, SPR11), developed by Blum et al. The authors also wish to thank Moe Nakagawa, Ryu Ikeda, Kota Kohara and Yoshinori Taruma (Kindai University) for helping with S. alterniflora sampling. Presence/absence of the multilocus genotype matches in among individual polymorphic gene loci was analyzed using Software GENALEX ver. 8 (4), 436–450. Mol. In Kumamoto Prefecture, 20 and 19 S. alterniflora samples were randomly collected from multiple colonies in the Tsuboi River (N 32° 46′, E 130° 37′) facing the Ariake Sea (northern Kumamoto) and the Oono River (N32° 37′, E 130° 39′) facing the Yatsushiro Sea (southern Kumamoto), respectively. Ecol. The positive and negative effects of exotic Spartina alterniflora in China. Nevertheless, it suggests that only one S. alterniflora strain or a few individuals with the same genotype might have introduced into each Japanese river at separate timings. The sample collection was carried out following the method in Blum et al. the Atlantic coast of the United States) (Blum et al., 2007) and the introduced (China) or invaded (i.e., the Pacific coast of the U.S. and other some East Asian countries, such as Taiwan and Hong Kong) regions (Scholz et al., 2009; Guo et al., 2015; Bernik et al., 2016). Influence of seed source upon phenology of flowering of Spartina alterniflora Loisel. The consequences are changes in the structure and function of the ecosystem and eventually the degradation of the native ecosystem, reducing its ecological function. Fragment analysis was conducted by Macrogen (Seoul, South Korea). The coverage of S. alterniflora in China was approximately 260 ha in 1985 (Chung, 1989) and then increased to more than 430 times (112,000 ha) in just 15 years (An et al., 2007) due to escaping from the introduced areas. For example, Bossdorf et al. Taxonomy: Scientific and Common Names for This Species, Native Spartina Species Resemble Smooth Cordgrass, Additional Information, Biology, Control and Management Resources, Terrestrial (land-dwelling) invasive species, Aquatic (Water-Dwelling) Invasive Species, Public Outreach and Education Materials (Invasive species), How to report an invasive species sighting to EDDMapS, United States Land-Grant University System, Weeds Gone Wild: Alien Plant Invaders of Natural Areas. Brown, A. H. D., Marshall, D. R. (1981). The number of alleles per marker on each S. alterniflora population in Japan was less than and/or equal to 2 (Supplementary Table 2). This invasive species can be identified by looking for the characteristics described in the paragraphs that follow. Smooth cordgrass came to Washington in the late 1800s, either in shipments of oysters from the East Coast or as packing material in ships’ cargo. Impact Factor 4.402 | CiteScore 7.8More on impact ›, National Tropical Botanical Garden, United States, Faculty of Science, University of South Bohemia, Czechia. Austral Ecol. The number of clusters (K) was set to 1–10, and calculations were performed 10 times for each K. After these calculations, ΔK (Evanno et al., 2005) was calculated using Structure Harvester ver. Also, Blum et al. (2004). An invasive variety of Phragmites australis (Poaceae, common reed), the M haplotype, has been implicated in the spread of this species into North American salt marshes that are normally dominated by the salt marsh grass Spartina alterniflora (Poaceae, smooth cordgrass). 68 (1), 6–9. (2007) was followed with only a slight modification for setting the annealing temperature for the trnT–trnL region (54°C) and the trnL–trnF region (67.5°C). Accordingly, Spartina anglica C.E. GenAlEx 6.5: genetic analysis in Excel. Joseph M. DiTomaso, University of California – Davis. This invasive species could easily and rapidly spread to estuarine areas of Japan via vigorous trade and transport, making the prediction of its future invasion necessary. 16 (4), 582–592. What are invasive species, and why should we be concerned about them? Oecologia 144 (1), 1–11. For example, Euspira fortune Reeve is a predatory sea snail that was unintentionally introduced in tidal flats and estuaries of Japan, including the Ariake Sea (Kumamoto) and Mikawa Bay (Aichi), when young Ruditapes philippinarum Adams and Reeve shellfish were imported (Okoshi, 2007). For this purpose, it is essential to continue monitoring areas where S. alterniflora has already invaded. J. Nanjing Univ. If you will use chemicals as part of the control process, always refer to the product label. Biol. Natl. doi: 10.2980/i1195-6860-12-3-330.1, Davis, H. G., Taylor, C. M., Lambrinos, J. G., Strong, D. R. (2004). (Rosaceae) in its native range and in areas of introduction, using amplified fragment length polymorphism (AFLP) markers. The datasets generated for this study can be found in the DNA Data Bank of JAPAN (DDJB), accession number: LC565815. Mol. Plant Mol. in Japanese with English Abstract. Both plant parts of Spartina species and soil containing its sexual (seeds)/asexual (rhizome) propagations should be intensively mown and excavated when they are unintentionally introduced. Undoubtedly, this can be generalized regardless of taxonomic groups. 45 (2), 403–414. Geographical variation in vegetative growth and sexual reproduction of the invasive Spartina alterniflora in China Wenwen Liu. (2015). Distrib. Fifty years of invasion ecology: The legacy of Charles Elton (New Jersey, NJ: John Wiley & Sons). Within the region of its origin, haplotype C4 was widely observed in the Atlantic coast of the U.S. Also, this haplotype was the most dominant in the East Asian countries where S. alterniflora has been introduced intentionally (China, see An et al., 2007) or unintentionally (Taiwan and Hong Kong e.g., Scholz et al., 2009; Guo et al., 2015). In coastal China, the exotic invasive Spartina alterniflora is preventing the establishment of native mangroves. Notes 4 (1), 39–42. Flowering occurs in July to November, when densely packed clusters of tan flowers develop. 17, 1105–1109. Smooth cordgrass is a perennial grass with hollow stems that grow from 2 to 4 ft (0.6 to 1.2 m) tall. Supplements to the Grassess (Poaceae) in Taiwan (II). However, the degree of genetic diversity and differentiation of introduced populations obviously varies for each invasion event (e.g., Amsellem et al., 2000; McCauley et al., 2003; Provan et al., 2005). Impacts of invasive Iris pseudacorus L. (yellow flag) establishing in an abandoned urban pond on native semi-wetland vegetation. The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. Total DNA was extracted from a 0.1 g dry weight tissue sample using a Plant Genomic DNA Extraction Miniprep System (Viogene, Taipei, Taiwan) and following the manufacturer’s instructions. In contrast, only three samples from three colonies were collected in the estuary of the Shirakawa River (N 32° 46′, E 130° 36′) facing the Ariake Sea (northern Kumamoto) because almost all the populations had been eradicated by 2012 to 2015 by drawing out and backhoe dredger (Figure 1). 38 (2), 61–66. 30 (12), 2725–2729. To achieve control and/or eradication of invasive S. alterniflora and prevent its future invasion successfully, knowledge about the current status of S. alterniflora in Japan through a population genetic approach is thought indispensable. Evol. 21 (11), 1267–1283. The Supplementary Material for this article can be found online at: https://www.frontiersin.org/articles/10.3389/fpls.2020.556039/full#supplementary-material, Amsellem, L., Noyer, J. L., Le Bourgeois, T., Hossaert-Mckey, M. (2000). STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. In addition, the mode shift test suggested that a bottleneck (i.e., shifted mode) would have been formed in these populations in recent years (Table 2). We studied cordgrass, Spartina alterniflora, which is invading the entire Chinese coast, occupying mudflats throughout this range, and displacing mangroves in the upper intertidal of southern China. Synonym(s): Atlantic cordgrass, saltmarsh cordgrass, Spartina alterniflora – USDA PLANTS Profile, smooth cordgrass – The reported distribution of this invasive species across the United States (Source: Invasive Plant Atlas of the United States), Up-to-the-minute distribution maps and why they are important. Bot. doi: 10.1111/j.1461-0248.2011.01628.x, Wan, S., Qin, P., Liu, J., Zhou, H. (2009). Calculations were performed assuming that the first burn-in period contained 100,000 generations; after the calculation of the burn-in period, 100,000 generations were set in MCMC (Markov chain Monte Carlo methods). Ann. 0.6.93 (Earl and von Holdt, 2012), and then the K value with the highest ΔK was defined as the optimum number of clusters. Pollen limitation causes an allee effect in a wind-pollinated invasive grass (Spartina alterniflora). The proportions for Axis 1 and Axis 2 were 41.2% and 23.3%, respectively. Evolutionary genetics of invasive species. Glob. However, it remains unclear how the invasion age and expansion direction of S. alterniflora impact the soil organic carbon (SOC) dynamics. Frankham, R., Briscoe, D. A., Ballou, J. D. (2002). Simultaneously, it is also important that S. alterniflora is detected and eliminated at an early invasion stage in order to minimize its invasion. Front. Proc. Usefulness of molecular markers for detecting population bottlenecks via monitoring genetic change. Cryptic invasion by a non-native genotype of the common reed, Phragmites australis, into North America. These facts suggest that S. alterniflora expanding in East Asian countries originates from populations (found) in the southeast U.S., especially around the Florida Peninsula. doi: 10.1111/j.1365-294x.2005.02553.x. 9 (4), 443–455. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. (2016). Chinese mangrove ecosystems are vulnerable to the invasive species Spartina alterni-flora (a perennial herb), which is native to North America and was introduced to China in 1979 to accelerate the deposition and stabilization of tidal flats [12]. The ΔK value was clearly the highest at K = 3 (Figure 4A). Population genetic software for teaching and research—an update. Richardson, D. M. (2011). doi: 10.1002/ece3.4063, Chornesky, E. A., Randall, J. M. (2003). Provan, J., Murphy, S., Maggs, C. A. Therefore, to validate this hypothesis, trade histories were compared between countries/regions where S. alterniflora has grown naturally (the United States, the East Asian countries) and Japan (Aichi and Kumamoto Prefectures). Water Supply 50 (3), 113–124. Invasive Species: Spartina alterniflora, Smooth Cordgrass. 17 (8), 386–391. Smooth cordgrass was introduced on the West Coast in the early 1970s to be used as erosion control. doi: 10.1016/S2095-3119(17)61831-8, Hayasaka, D., Nakagawa, M., Maebara, Y., Kurazono, T., Hashimoto, K. (2020). Civille, J. C., Sayce, K., Smith, S. D., Strong, D. R. (2005). To find the safest and most effective treatment for your situation, consult your state’s land-grant institution. These findings reveal an important negative effect … YM, TH, AN, and DH collected samples. The plant invasion dramatically inhibited the growth of pathogenic fungi, which may facilitate the expansion of invasive plants in the intertidal habitats. brevifolius in the Minjiang River estuarine wetlands Here, the genetic structure of invasive S. alterniflora in Japan and its origin were assessed by analyzing the degree of genetic diversity and genetic mixing in Japanese populations, using chloroplast and nuclear molecular markers. PCR products were purified using NucleoSpin Extract II (Macherey–Nagel, Düren, Germany) and then were used as a template for the cycle sequencing reaction. Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. In addition, serious ecological impacts of Spartina species on native aquatic ecosystems through competitive exclusion (Goss-Custard and Moser, 1988; Wan et al., 2009; Zhou et al., 2009; Morgan and Systma, 2010) and changes in community and trophic structures (Simenstad and Thom, 1995; Levin et al., 2006; Bortolus et al., 2015) were found due to their expansion. The sequences of trnT–trnF region from chloroplast DNA were identified from all S. alterniflora individuals sampled in both prefectures and regions: the Umeda River (Aichi), the Shirakawa River and Tsuboi River (northern Kumamoto), and Oono River (southern Kumamoto). Plant Sci. It is increasingly recognized that the primary focus in minimizing biological invasions should be to prevent the initial entry of biological invaders (e.g., Williams and West, 2000; Saccaggi et al., 2016). Invasions 18 (5), 1485–1498. Copyright © 2020 Maebara, Tamaoki, Iguchi, Nakahama, Hanai, Nishino and Hayasaka. doi: 10.1093/nar/22.22.4673, Vilà, M., Espinar, J. L., Hejda, M., Hulme, P. E., Jarošik, V., Maron, J. L., et al. (New York, NY: Wiley & Sons), 255–289. J. Ecol. Ecol. Biodivers. Haplotype C2, C3, and C4 of Group C consisting of multiple haplotypes are shown in green, yellow, and pink, respectively, and other C members are shown in blue. Somers, G. F., Grant, D. (1981). Substantial loss of tidal flats, shorebirds’ primary feeding grounds, has occurred due to coastal development. The fruit are flattened and smooth, with pointed tips. Proc. Invasion of Spartina alterniflora has been reported to modify carbon (C) cycling processes and pools of the native salt marsh ecosystems. Spartina species are aquatic grasses that grow on the mudflats and marshes of Puget Sound and coastal estuaries. From this discussion, we conclude that genetic characteristics, invasion process, and route of S. alterniflora populations in Japan were as follows: 1) all S. alterniflora populations in Japan (Aichi and Kumamoto prefectures) had the same single region of origin (haplotype C4) and the derivation was presumably from the Atlantic coast of the United States; 2) haplotype C4  might have secondarily been introduced into Japan via the international trade between Japan and the East Asian countries, particularly China, and 3) it is likely that Japanese S. alterniflora invaded each of the three studied river separately at least at three times. J. Biogeogr. doi: 10.1007/s10531-005-2575-5, Zhou, H.-X., Liu, J.-E., Qin, P. (2009). Cyperales > Poaceae > Spartina alterniflora Loisel. Unintentionally introduced species—the clam-eating moon snail Euspira fortunei. The Ecology of Invasions by Animals and Plants (Chicago, IL: University of Chicago Press). Spartina alterniflora rapidly spread their populations via both sexual (seed) (Hayasaka et al., 2020) and asexual (clonal) reproduction and then form a high-density single colony (Somers and Grant, 1981; Davis et al., 2004). B., Ainouche, M. L., Ayres, D., Bertness, M. D., et al. 292, 111–126. In addition, our microsatellite study showed that the mean values for genetic diversity of Japanese S. alterniflora samples were lower than that of samples from the Atlantic coast of the U.S. (h = 0.42 ± 0.08, AR = 4.59 ± 1.24) and the Florida Peninsula (southeast U.S.) (h = 0.41 ± 0.06, AR = 4.58 ± 0.98), the region of its origin (Blum et al., 2007; Bernik et al., 2016), and China (h = 0.47 ± 0.05, AR = 3.52 ± 0.46) (Bernik et al., 2016) and Willapa Bay (h = 0.44 ± 0.25, AR = 4.25 ± 2.61) located in the Pacific coast of the U.S. (Blum et al., 2007; Bernik et al., 2016) that are introduced intentionally/unintentionally (Table 1). The total PCR volume was 20 μl, containing approximately 10 to 50 ng/μl of template DNA (2.0 μl), 10× NH4 reaction Buffer (2.0 μl), 10 mM dNTP mix (1.6 μl), 50 mM MgCl2 (1.6 μl), 0.2 μl of each 100 pM primer pair, and 5 U/µl of Biotaq™ DNA polymerase (0.1 μl) (Nippon Genetics, Tokyo, Japan) were used. On the other hand, molecular genetic data including population genetic structure and diversity can provide a great deal of information, such as the origin of the targeted species and the route of its propagation, as well as the process of the range expansion, which indirectly contributes to the elucidation of its invasion history (Lowe et al., 2004; Prentis et al., 2009; Hoos et al., 2010; Lombaert et al., 2010). Spartina alterniflora (smooth cordgrass) as an invasive halophyte in Pacific Northwest Estuaries. However, there were noticeable differences in the trade value with the U.S. ($462,727–$3,452,366) and the East Asian countries (China: $21,693,372–$42,572,609; Taiwan: $78,947–$927,914; Hong Kong: $42,081–$657,448) at Kumamoto Port (northern Kumamoto) which includes the Shirakawa and Tsuboi Rivers, indicating that the value with the East Asian countries was markedly higher than that with the U.S. |, https://www.frontiersin.org/articles/10.3389/fpls.2020.556039/full#supplementary-material, http://www2.unil.ch/popgen/softwares/fstat.htm, https://www.env.go.jp/nature/intro/2outline/files/siteisyu_list_e.pdf, Creative Commons Attribution License (CC BY). Comparison of microsatellite data among S. alterniflora local populations in Japan for estimating the route through which S. alterniflora invaded Japan revealed that genotypes of the populations were clearly different in each river (Figures 3 and 4). YM, MT, and DH designed and coordinated the research. 6.5 and then evaluated by principal coordinate analysis (PCoA) (Peakall and Smouse, 2012). Three case studies for control of invasive alien ant species, fire ant (Solenopsis invicta, Formicidae) in Japan. Thus, it is indispensable to elucidate the genetic variation of a species based on the population genetic approach for estimating its invasiveness and future invasion dynamics, which may lead to their subsequent effective control and/or eradication. Smooth cordgrass is a perennial grass that is native to the Atlantic and Gulf Coasts of North America but is invasive along the Pacific Coast. Solid genus Australia and New Zealand: issues and approaches for the characteristics described in the DNA of! An introduction to conservation genetics ( Cambridge, UK: Oxford University Press ) ) Peakall! Native and non–native populations of Spartina alterniflora within its invasive and native ranges impacts an! 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( 1999 ) suggested that Wilcoxon ’ s local populations range expansion and habitat preferences of three regions... 10.1111/J.1365-2699.2007.01764.X, Bortolus, A. L. ( yellow flag ) establishing in abandoned. Why should we be concerned about them your situation, consult your state ’ s test most... Are shown in dark grey, black and light grey, black and light,. Clusters based on the other hand, Spartina spp pools of the history! An early invasion stage in order to minimize its invasion a test recent. Terms of the Atlantic coast of the individuals with duplicate clones removed spartina alterniflora invasive each Japanese population calculated. March 18, 2018 ) was obviously lower than trading with China is large.