Hydrobiologia (2014) 741:101–111 DOI 10.1007/s10750-014-2012-4 CHALLENGES IN AQUATIC SCIENCES Effect of the invasive bivalve Mytilopsis sallei on the macrofaunal fouling community and the environment of Yundang Lagoon, Xiamen, China L.-Z. Cai • J.-S. Hwang • H.-U. Dahms • S.-J. Fu • Y. Zhuo • T. Guo Received: 28 January 2014 / Accepted: 9 August 2014 / Published online: 24 August 2014 Ó Springer International Publishing Switzerland 2014 Abstract Mytilopsis sallei is a small marine bivalve with season and with station. The species diversity of and is considered as a serious pest. We assume that the the macrofaunal fouling community at stations B and invasive bivalve M. sallei changed the community F was low in summer, because high density of M. structure of fouling macrofauna and reduced the sallei was found at two stations. There were signifi- species diversity index in Yundang Lagoon, Xiamen, cantly positive correlations between density and China. In order to verify the above hypothesis, test biomass of M. sallei and water temperature and panels were submerged seasonally at five stations COD, and significantly negative correlations with pH. during four seasons in Yundang Lagoon, and some The results confirmed that this invasive species chemical parameters were determined. The results changed the density and biomass compositions of showed there were significant differences in density fouling macrofauna, reduced the species diversity and biomass of M. sallei and other fouling macrofauna index during the summer period, and somewhat worsened the aquatic environmental quality in Yund- ang Lagoon, because the pH and the DO were the Guest editors: Jiang-Shiou Hwang & Koen Martens / lowest, and the BOD and the COD were the second Challenges in Aquatic Sciences lowest in summer among four seasons. & L.-Z. Cai ( ) Á S.-J. Fu Á Y. Zhuo Á T. Guo Keywords Invasive species Á Mytilopsis sallei Á College of the Environment and Ecology, Xiamen University, Xiamen 361102, China Macrofaunal fouling community Á Aquatic ecosystem Á e-mail: [email protected] Xiamen Yundang Lagoon J.-S. Hwang Institute of Marine Biology, National Taiwan Ocean University, Keelung 202, Taiwan, ROC Introduction H.-U. Dahms Department of Biomedical Science and Environmental The introduction or immigration of foreign species Biology, Kaohsiung Medical University (KMU), No. 100, Shin-Chuan 1st Road, Kaohsiung 80708, Taiwan, ROC is a major cause of biodiversity loss (Crooks, e-mail: [email protected] 2002). The impact of alien species might affect three major biodiversity aspects: species, their H.-U. Dahms genetic structure, and landscape (Wiegleb et al., Department of Marine Biotechnology and Resources, National Sun Yat-sen University (NSYSU), No. 70, 2013). Among bivalves, some dreissenids have Lienhai Road, Kaohsiung 80424, Taiwan, ROC become invasive pests when being introduced to 123 102 Hydrobiologia (2014) 741:101–111 or invading new environments (Kennedy, 2011a). Since the discovery of M. trautwineana within a As sessile suspension feeders, dreissenid and my- shrimp farm at the Caribbean coast of Colombia, the tilid bivalve molluscs have become some of the mussel has reached high abundances in the beds of most important invasive organisms in marine, some ponds, where it builds up layers of up to 10 cm brackish, and freshwater ecosystems (Aldridge (Aldridge et al., 2008). et al., 2008). Mytilopsis sallei has successfully From mussels to barnacles to algae, studies suggest invaded several major ports in East Asia (Wong that such ‘‘hull-fouling’’ organisms could pose an et al., 2011). M. sallei was reported in an oyster invasion threat that is ‘‘equally strong if not stronger’’ bed at Tapeng Bay, near Tungkang Port, in Taiwan, than that from organisms transported by ballast water in 1977 (Chang, 1985) and in Kiyomizu harbour, (Dahms et al., 2004a; Strain, 2012). M. leucophaeata Japan, in 1979 (Ishibashi & Kasaka, 1980). M. usually occurs in very low numbers and has rarely sallei was collected alive from Hong Kong waters been mentioned in field survey reports; However, (Tolo Harbour) attached to a floating wreckage occasionally in its native habitat and often in habitats (Morton, 1980). M. sallei was introduced to Maluan where it has been introduced (as in Europe and Brazil), Bay in Xiamen as feed for cultured fishes and it may undergo population break-downs for no clear shrimps at the beginning of the 1990s, and soon it reason (Kennedy, 2011a). became a dominant species within its fouling To assess the invasive ability of M. sallei, both community (Wang et al., 1999). A high mortality spatial and temporal variables should be considered. of Balanus reticulatus was noted when M. sallei Local biotic effects such as on top-down control by occurred at high density in Maluan Bay, Xiamen, predatory fish and any relationship to the benthic China (Cai et al., 2005, 2006). The Caribbean false community need to be surveyed and then be mussel M. sallei (Re´cluz, 1849) occurs in tropical extrapolated to the entire ecosystem (Karatayev monsoon drains of Singapore (Tan & Morton, et al., 2007). This particularly holds for the 2006). M. sallei colonized Yundang Lagoon in the suspension-feeding ability of M. sallei (Borthagaray year 2000 (Cai et al., 2010). The bivalve M. sallei & Carranza, 2007). The system-wide effects depend was reported as an invasive species in Indian not only on the characteristics of the water bodies waters (Gaonkar et al., 2010a, b). In the south- (invasibility), but also on the invasiveness of M. western region of Taiwan, M. sallei causes not only sallei. Its initial impact is expected to be modified abundance declines of native hard clam, but also over time (Hicks, 2004). undesirable changes in aquaculture systems and Predicting the ecosystem consequences of simulta- economic losses (Liao et al., 2010). neous gains (invasion) and losses (extinction) requires Other species of the genus Mytilopsis were found that we first understand which biological traits abundantly in several countries. Conrad’s false mus- predispose life forms to higher probabilities of extir- sel, M. leucophaeata, is a highly euryhaline species, pation or establishment (response traits), and detail originating from the Atlantic coast of the United States how response traits covary with traits that drive and the Gulf of Mexico (Marelli & Gray, 1983, 1985), ecosystem functioning (effect traits) (Cardinale 2012; and now settles in industrial cooling water systems in Wiegleb et al., 2013). We assume that the invasive Europe (Jenner et al., 1998), with settlement densities bivalve M. sallei changed the community structure of as high as 5.5 million m-2 (Rajagopal et al., 2003). fouling macrofauna (the proportions among fouling Rajagopal et al. (1997) reported M. leucophaeata to be macrofauna groups), reduced the species diversity the dominant macrofouling organism of electricity- index, and increased some chemical materials in generating stations in the Noordzeekanaal of the Yundang Lagoon, Xiamen, China. Following this Netherlands. Laine et al. (2006) reported that M. hypothesis, the present study aims to analyze the leucophaeata was near a power plant’s cooling water temporal and spatial distribution of M. sallei and the discharge in the Baltic Sea. Originating from the relationship between density and biomass of M. sallei Pacific coast of Panama, M. adamsi appeared later in a and environmental factors, as well as between M. shrimp farm along the Pacific coast of Mexico sallei and other fouling macrofauna in Yundang (Salgado-Barraga´n & Toledano-Grandos, 2006). Lagoon, Xiamen, China. 123 Hydrobiologia (2014) 741:101–111 103 Fig. 1 Panel test stations for fouling macrofauna in Yundang Lagoon, Xiamen, China Materials and methods two panels after retrieval at a panel station. Each panel measured 20 cm 9 20 cm 9 2 cm. Study site All samples and retrieved panels were immediately fixed in 5% formalin until examination in the labora- Yundang Lagoon (24°290N, 118°040E), which used to tory. In the laboratory, the samples were sieved be a natural bay called Yundang Harbour, is located in through a 0.5 mm mesh. Fouling macrofauna retained the western bay of Xiamen, China. Since the early on the sieve was stored in 70% ethanol. Fouling 1970s, a great number of land reclamation projects macrofauna was identified to species level or to the were carried out by the Xiamen government, and the lowest taxonomic level possible, e.g., genus, which Yundang Harbour gradually became an almost-closed was then treated as a distinct taxon in the analysis. salt lake, with its area reduced from the original 10 to Fouling macrofauna was counted under a dissection 2.2 km2. Floodwater draining channels in the urban microscope and weighed using an electronic balance district were built along the site of Yundang Lagoon. (sensitivity as 0.1 mg) (see Dahms et al., 2004b). A sea wall was constructed to keep Yundang Lagoon Eight environmental factors, i.e., water tempera- from the Western Sea of Xiamen. However, in order to ture, salinity, pH, DO (dissolved oxygen), BOD circulate the water, the incoming waters of natural (biochemical oxygen demand), COD (chemical oxy- tides were utilized by regulating the water gate gen demand), NH3-N (nitrate nitrogen), and DIP diurnally. This way of circulating seawater was (dissolved inorganic phosphate = reactive phosphate) transported by tidal force. The circumference of were calculated for every sampling (see Dahms & Yundang Lagoon is now a main shopping center, Qian, 2005). residential area, and recreation park of Xiamen. Statistical analysis Field methods The species diversity index of each station was Five stations, identified as B–F, were investigated in calculated using Shannon–Weaver index (H0). terms of fouling macrofauna that settled on pine test Multi-factorial Analysis of Variance (ANOVA) panels (Fig. 1). Station B was at the drainage channel; from SPSS software was used to investigate differ- more residential sewage outlets were there. Station C ences between seasons (summer, winter, spring, and was at an inner lake.