**4. Discussion**

For the first time, this study assesses the trophic features and benthic diversity of the Yundang Lagoon, an urban coastal lagoon in Southeast China, in a comprehensive and integrated manner. The Yundang Lagoon was referred to as a "dead" lagoon in the 1970s, and has undergone 30-year restoration e ffort. Microbiological and eco-toxicological studies conducted in the last decade sugges<sup>t</sup> that the recovery of the Yundang Lagoon has not ye<sup>t</sup> been accomplished. In particular, high levels of heavy metals and estrogenic compounds originating mainly from municipal wastewaters have been found in sediments and pore-water of the Yundang Lagoon posing serious toxic risk to the biota including humans [44–46]. Furthermore, evidence has shown that the discharge of surrounding sewage is still a major source of OM pollution in the Yundang Lagoon [34,46].

These results provide a detailed analysis of the trophic features of the Yundang Lagoon and highlight the high spatial heterogeneity of both abiotic (water and sediments) and biotic (macrozoobenthos) components, in spite of its small size and the absence of a salinity gradient. From an abiotic perspective, both water and sediment variables independently point in the same direction. In particular, there was a major separation between the low-nutrient and sandier sites A and B in the outer sector of the lagoon, and the hypertrophic and organically over-enriched site F in the inner canal. Site F departed the most from all the other sites, which was consistent with the fact that this sector of the lagoon is still subjected to numerous sewage discharges [32,47]. The confined location and reduced hydrodynamics of site F are indicated by high levels of suspended solids in the near-bottom water and a high silt content in surface sediments, making the site likely to favor the accumulation of toxic by-products derived from the microbial decomposition of high amounts of OM which were present above established critical thresholds [24,25]. Indeed, higher BOD5 and CODMn concentrations measured at this site (where we also observed methane bubbling from the sediment) may be a concurrent evidence of high saprobity levels in this sector of the lagoon which, in turn, will severely a ffect the biota [18]. On the other hand, all other sites of the lagoon showed significantly lower Chl-*a* (in water) and TOC (in sediment) concentrations than those found at site F, notwithstanding seasonal variation, which was not considered here, during phytoplankton blooms [34]. Interestingly, our results are consistent with those reported by Sun et al. [33] who found spatial variation in Chl-*a* and TOC to be greater in highly urbanized watersheds such as Yundang Lagoon, than in less urbanized watersheds. Overall, our study demonstrates that at the time samples were taken for this study (2012), the Yundang Lagoon had much lower nutrient, BOD5, and CODMn concentrations than those found in previous decades [29], supporting the inference that a partial, but significant environmental recovery has occurred.

The overall improvement of the environmental condition of the Yundang Lagoon was reflected in a major recovery and revitalization of the lagoon's soft-bottom benthic assemblage during the last decade. Following anoxic and azoic sediments found when the lagoon was highly polluted and closed to the adjacent coastal waters until 1987 [29], a single polychaete species, *Neanthes succinea*, typical of organically enriched sediments with high H2S content [14,48], was reported during the first phase of the restoration program (1989−1992). Between 2001 and 2008, nine species started to colonize the lagoon's sediments [43]. Among them, the opportunistic polychaetes *Capitella capitata* and *Neanthes glandicincta*, typical of muddy, organically enriched sediments were dominant, while they occurred with few individuals in our study. These results show a significant recovery of the macrozoobenthic assemblages for the first time, with a marked increase in species richness and diversity, ye<sup>t</sup> a heterogeneous distribution across the lagoon. Of the 43 species found, eight were dominant (accounting for 93% of the total abundance), mainly represented by mollusks and amphipods, and including the polychaete *Cossurella dimorpha* which was not reported previously. Overall, the most dominant species was the bivalve Dreissenidae *Mytilopsis sallei*, an invasive alien species native to the Caribbean and a massive component of fouling events [49,50]. *M. sallei* was transported to China via ballast waters, and was first recorded in Xiamen waters (Maluan Bay) in 1990 and in the Yundang Lagoon in 2000 [51–53]. In a basin as small as the Yundang Lagoon, one may expect little spatial

variation in the soft-bottom benthic assemblages. However, our extensive sampling effort allowed us to identify significant variation in the macrozoobenthic assemblages within relatively short distances of a few hundred meters. A number of environmental and biological factors may help explaining the high spatial variability and the recovery of the macrozoobenthic assemblages in the Yundang Lagoon. These are: (1) the heterogeneous morphology and the peculiar hydrology of the lagoon, including the daily water exchange with the adjacent coastal sea, (2) the high environmental variability in water and sediments across the lagoon, (3) the presence of nonpoint sources of pollution and other anthropogenic pressures, and (4) the dominance of the invasive *M. sallei* and the biotic interactions within the benthic community. Thus, the present work represents a unique case-study to evaluate the complex dynamics of macrozoobenthic assemblages in a formerly dead urban coastal lagoon following long-term restoration.

As an example, sites A and B in the outer sector of the lagoon, although similar in several environmental features and, thus, significantly different from the other sites, were the least similar to one another in terms of benthic species composition, richness and diversity. In particular, site A was the most abundant, biomass-rich, and species-rich site in the lagoon, while the opposite was true for site B, which had a species richness and diversity as low as that found at the most degraded site, F. We infer that such biotic differences between sites A and B may be related to their position within the outer sector of the lagoon. In particular, site B was located near the heavily modified shoreline made by a concrete wall, following earlier dredging and reclamation, which may have left little of the historic ecohydrological system on this site of the lagoon. This may have contributed to determine a poor macrozoobenthic assemblage which included few species typical of muddy sediments, such as *Cossurella dimorpha*, *Corophium* sp. and *Gammaropsis* sp. On the other hand, site A was located closer to the shoreline where mangrove species, such as *Kandelia candel*, *Avicennia marina*, *Rhizophora stylosa*, and *Heritiera littoralis*, had been successfully planted from 2001 to 2006 [54], contributing to increases of birds and fish species in the lagoon [29]. It is likely that the presence of mangroves along this shore has favored the colonization of the invasive fouling species *M. sallei*. This bivalve was associated with the richest benthic assemblage of the lagoon, correlating with the highly diverse assemblages found at site A which also included species typical of mangrove habitats such as *R. plicatula* and *S. glabra*. The diversity of the site was also seen in *Corophium uenoi*, which lives within muddy tubes on soft bottom sediments, but is also present in the fouling community, and *P. tsurumaru*, which is typical of muddy sediments and possibly shares the burrow of holothurian or crabs (commensal). On the contrary, the innermost site F had the most impoverished assemblage, consistent with its degraded condition in both water and sediments. Yet, *M. sallei* was also found at one station at this site, providing evidence of its high resistance and resilience, and its ability to settle when a substrate is available, owing to the characteristic traits of opportunistic *r-*strategists [49,50]. The apparently random distribution of *M. sallei*, heavily colonizing some sectors of the lagoon, was also indicated by its dominance at site C, where environmental conditions were intermediate between the outer (sites A and B) and the innermost (site F) sectors. This indicates that, in addition to the environmental factors, species-specific biological interactions should be considered to evaluate the complex dynamics that occur within a benthic assemblage.

Our results sugges<sup>t</sup> that *M. sallei*, known as an invasive ecosystem engineer that creates new habitats and favors the settlement of other species [55], may support a rich and diversified community. In particular, in the present study *M. sallei* was associated with the highest number of species having different biological traits (e.g., fouling, parasite and commensal) and typical of different habitats (e.g., muddy sediments, mangroves). Among them, *S. glabra*, an IUCN threatened species [56] in need of protection measures, and *P. tsurumaru* which is known to establish symbiotic relations with other species [57]. Nevertheless, *M. sallei* is also well known as a pest species characterized by wide temperature, salinity, and oxygen tolerances, as well as a fast growth-rate and a high fecundity which may favor competition with native species and inhibit the growth of other species [49]. As an example, an experimental field study on the fouling macrofauna associated with *M. sallei* conducted in the

Yundang Lagoon showed a reduction in species diversity in summer when environmental conditions worsened, but the density and biomass of both *M. sallei* and fouling macrofauna were highest [52]. Furthermore, *M. sallei* is known to erode fishing facilities and artificial structures leading to ecosystem damage, economic loss, and inconvenience to locals [53], thus, its spatial and temporal variation should be carefully monitored.

With regards to the spatiotemporal evolution of the macrozoobenthic assemblages in the Yundang Lagoon, one possibility is an even more massive colonization of the lagoon by *M. sallei* as the most dominant species. The successful establishment of *M. sallei* in the Yundang Lagoon may prefigure a wider, ye<sup>t</sup> probably overlooked colonization of this species as a structural component of the benthic assemblages in other Chinese coastal waters and lagoons for which information is very scant [53]. A similar colonization process occurred in the Mediterranean Sea during the first half of the last century by Serpulidae *Ficopomatus enigmaticus* which is now a typical bioengineer species in Mediterranean lagoons [58–60]. However, after a period of dominance, *M. sallei* may decrease in dominance or even be replaced by other species typical of sessile fouling, such as *S. plicata*. A similar alternation of species has been found between the mussel *Mytilus edulis* and the polychaete *Sabellaria spinulosa* along the eastern Atlantic coast, and in the Mediterranean Sea between *M. galloprovincialis* and the extensive bioconstructions of *S. spinulosa* along the Italian Puglia coast [61,62].
