Spartina anglica density, height, coverage, and biomass
Our results showed that the structural characteristics of invading Spartina patches, including living leaf biomass, rhizome biomass, and coverage, were dependent on Spartina patch size. Small patches had significantly higher rhizome biomass than medium-sized and large patches at depths of 0–10 cm. Patch size is related to invasion history: smaller patches indicate a shorter invasion history. Therefore, we assume that changes to S. anglica structural characteristics occur after invasion and spread throughout the patches.
At the study area, Spartina anglica patches with a short invasion history allocated resources to roots and rhizomes, to settle early populations and adapt to harsh environmental stresses such as high salinity and tides. Schubauer and Hopkinson (1984) also reported that rhizomes accounted for a greater portion of belowground biomass in a Georgia salt marsh. Investment of resources into rhizomes is crucial for the invasion of clonal plants, such as S. anglica, allowing them to adapt to a wide range of habitats by maintaining soil volume (Petrone et al. 2001). If belowground organic matter accumulation is insufficient, marshes with abundant aboveground plants can rapidly become open water, as accumulated sulfide causes plant death. Clonal integration is an important means of population expansion for the invasive Phragmites australis, which would otherwise be confined to higher-elevation marshes due to low oxygen availability at lower elevations (Amsberry et al. 2000).
Table 2
Factor loadings of variables obtained by canonical correspondence analysis (CCA). Zonation was determined at standard error (SE) > 0.600 (bold).
|
CCA1
|
CCA2
|
Organic matter
|
–0.4199
|
0.3435
|
NH4-N
|
0.5127
|
0.6557
|
PO4-P
|
0.1575
|
0.3174
|
pH
|
0.6387
|
–0.2434
|
Salinity
|
–0.3880
|
0.2218
|
Belowground biomass
|
–0.9453
|
0.1326
|
Proportion of variance
|
0.5134
|
0.2681
|
Cumulative proportion
|
0.5134
|
0.7815
|
Eigenvalues
|
0.3819
|
0.1994
|
Aboveground and belowground biomass allocation are important for marsh ecosystem structure and function, because they influence various processes such as carbon sequestration, gas transport, nutrient cycling, and ecosystem resilience (Darby and Turner 2008; Tripathee and Schafer 2014; Castillo et al. 2016). The ratio of below- to above-ground biomass was significantly higher in small Spartina patches, suggesting differential carbohydrate use under harsh environmental condition (Castillo et al. 2016) despite its small range (0.13–0.16). In spring, high root and rhizome biomass can affect leaf biomass. Phragmites asturalis, Egertian densa, and Myriophyllum show depleted carbohydrate reserves in the rhizomes during rapid growth (Costa et al. 2003). Spartina alterniflora showed evidence of biomass translocation from below- to above-ground early in the growing season, when aboveground growth is at its maximum (Connor et al. 2000). However, the ratio of below- to above-ground biomass differed significantly according to settlement history and location within the marsh (Valiela et al. 1976; Roman and Daiber 1984; Wigand 2008). Dame and Kenney (1986) reported an average net aboveground primary production of 2,188 and 1,295 g m–2 year–1 at low and high elevations within the marsh, respectively, whereas the corresponding average net belowground primary production rates were 2,363 and 5,445 g m–2 year–1. Ellison et al. (1986) also reported decreasing root and rhizome penetration (< 20 cm) into the marsh substrate with increasing tidal height, and belowground biomass reached a maximum at the marsh edge.
In the present study, rhizomes sampled at depths of 6–9 cm were often curved, returning to the surface layer where they could become shoots. This finding indicates that depth should be considered as a major factor for the eradication of Spartina. Spartina densiflora is a halophyte with high salinity tolerance, but its growth is limited in halosaline conditions (Castillo et al. 2016). In the present study, salinity was not directly related to S. anglica biomass accumulation in any habitat; therefore, S. anglica may have greater salinity tolerance than S. densiflora.
Effect of Spartina invasion on macrobenthic communities
Intertidal macrobenthic communities usually vary by habitat type and tidal level (Hosack et al. 2006; Bouma et al. 2009; Compton et al. 2013). In the present study, the effects of Spartina on macrobenthic communities was estimated and compared to those in adjacent habitats. Plant introductions to salt marsh systems result in significant changes, ranging from species replacement to widescale alteration of ecosystem properties; these altered physical and chemical environments can also strongly influence the recruitment, survival, growth, and reproduction of benthic invertebrates in invaded areas. (Neira et al. 2005; Grosholz et al. 2009). Neira et al. (2005) observed 75% lower total macrofaunal density, and lower species richness, in Spartina-vegetated sediments representing 30-year-old invasion at Elsie Roemer Bird Sanctuary (California, USA) than in an adjacent unvegetated tidal flat. Differences in macrofaunal community structure have been shown to be greater among tidal elevations than between native halophyte and invasive Spartina communities in Chinese estuarine Spartina-invaded tidal flats (Chen et al. 2009). The present study also revealed a significant association between Spartina invasion and macrofaunal assemblages. We observed macrofaunal changes in bare mudflats and Suaeda vegetation invaded by Spartina, including low species richness, H’, and macrofaunal density; more epifauna in Spartina-invaded bare mudflats; higher density of the subsurface deposit-feeding nereidid polychaete Perinereis linea in Spartina-invaded Suaeda vegetation; and no significant difference in macrobenthic biomass among habitats. Spartina invasion also affected macrobenthic communities depending on the invasion history, which was estimated to be 2–5 years at the study site. Even within such a short period, the impact of S. anglica on macrofaunal diversity and density was sufficiently strong to produce significant effects. To some extent, these results are consistent with previous findings obtained in a temperate Australian salt marsh (Cutajar et al. 2012), and in Wenzhou Bay, China (Get et al. 2012). Cutajar et al. (2012) reported that invaded patches showed a 50% reduction in species richness, and reduced diversity, compared to two uninvaded habitats. Macrofaunal density in the S. anglica patches of the present study was also lower than that in native marsh (by 60%), but not significantly different from that in the bare mudflats. We observed no differences in biomass among habitats. Ge et al. (2012) demonstrated that macrobenthic communities were more complex in initial S. alterniflora invasion patches than in patches at other invasion stages, and that S. alterniflora invasion stage significantly affected macrobenthic community structure; their results also indicated higher biodiversity in the initial stage of invasion (1–2 years), decreasing during invasion progress (3–4 years) until completion (5–6 years), perhaps due to S. alterniflora canopy changes.
Our CCA results indicated that the key environmental factors driving macrobenthic ommunity changes were belowground biomass, organic matter content, salinity, and pH (Fig. 6). S. anglica invasion was associated with low pH, high organic matter content, high belowground biomass, and high salinity. These results are consistent with those of previous studies reporting changes in the physicochemical properties of sediment habitats under Spartina invasion (Neira et al. 2007). The macrofaunal diversity and density of tidal flat environments increase significantly when ecosystem engineers, such as oyster reef or seagrasses, are present because they create and modify habitat structures (Brusati and Grosholz 2006). In this study, comparison of macrofauna assemblages between habitats with and without Spartina patches showed clear trends (Fig. 6). Macrofaunal H’ was higher in bare mudflats and native marsh than in habitats containing Spartina patches. Spartina patches yielded low macrofaunal diversity, low and richness in mudflats (Hedge and Kriwoken 2000). However, the infaunal polychaete P. linea, and the epifaunal gastropods B. cumingi and L. takii, were enhanced in Spartina patches. These findings are similar to previous reports of increased macrofaunal dominance with a shift in feeding mode from surface microalgal feeding to subsurface detritus feeding (Neira et al. 2007; Bouma et al. 2010), which creates Spartina-free areas in open mudflats (Brusati and Grosholz 2009). In a study examining the influence of Spartina marshes and detritus availability on the spatial structure and temporal variability of macrobenthic associations, Netto and Lana (1999) suggested that spatial and temporal shifts among infaunal organisms may be more evident than those of mobile epibenthic forms.
Our study area contained no 2-cm-diameter burrows among Spartina patches, which indicates the absence of large decapod crustaceans; we also observed a higher density of Annelida than Mollusca organisms. Spartina patches appeared to facilitate the colonization of oligochaetes at higher elevations, while also inhibiting taxa such as crustaceans and bivalves. However, macrofauna biomass did not differ significantly between habitats with and without Spartina. This result is consistent with the findings of a study on the effects of Spartina invasion on benthic macrofaunal assemblages in an Australian salt marsh (Cutajar et al. 2012), but not with those of previous studies that found a negative correlation between root biomass and macrofaunal biomass (Forbes and Lopez 1990, Wang et al. 2010).
Our CCA results clearly showed that Spartina invasion was a key factor in macrofaunal distribution (Fig. 6). When belowground biomass was sufficient, macrofauna diversity, density, and richness decreased to a greater extent among Spartina patches, whereas a few species, such as epifauna, remained dominant. Macrofauna species may have been depleted compared to both native marsh and bare mudflats due to the belowground biomass of roots and rhizomes. Our CCA results also indicated that organic matter content, salinity, and pH can be considered as crucial factors for community organization. Benthic deposit feeders assimilate resuspended benthic diatoms from bulk particulate organic matter (Kang et al. 2003; Kanaya et al. 2008). Despite the high salinity tolerance of S. densiflora, its growth is limited under halosaline conditions; we found that salinity was positively related to belowground S. anglica biomass. Lee et al. (2016) demonstrated the high invasion potential of hybrid Spartina genotypes due to their strong salinity tolerance; plants under high salinity conditions had a significantly greater root to shoot biomass ratio than those under either low or medium salinity conditions. Interactions between pH and salinity are important for evaluating Spartina responses in nutrient culture and salt marsh experiments (Linthurst et al. 1981).
In conclusion, we investigated the effects of S. anglica patch size in a range of tidal flat marsh habitats, to understand its reproductive strategies throughout the invasion process and its influence on macrobenthic communities. Smaller Spartina patches, which indicate a shorter invasion history (1–2 years), allocated more resources to rhizomes than larger patches, to adapt to the harsh tidal environment. Spartina invasion reduced macrofaunal species richness, diversity, and density, but may have enhanced epifauna in the tidal flat marsh. Macrofaunal assemblages may have been negatively impacted in habitats under Spartina invasion; however, the results differed among habitat types. This study focused on early invasion Spartina patches rather than established meadows, to understand its initial asexual reproductive strategies and effects on macrofauna. Our results indicate that rhizomes in early S. anglica patches represent an important means of population expansion from favorable to unfavorable environments. Early detection and a rapid response are key for managing Spartina invasion, particularly within 5 years, when S. anglica invasion has a major negative impact on native microbenthic communities. Further studies should perform long-term (> 5 years) monitoring of Spartina invasion patterns and structural characteristics, and assess the impact on surrounding macrobenthic communities.