Response of meiofauna with special reference to nematodes upon recovery from anthropogenic activities in subtropical waters of Hong Kong

Abstract

Owing to their sessile mode of life, marine benthic communities have long been used as bioindicators for monitoring coastal pollution. In recent years, there has been an increase in the use of smaller-sized organisms, such as meiofauna (size 38 - 500 μm), as target organisms. Meiofauna offer many advantages as biological indicators. Specimens of meiofauna, especially free-living marine nematodes, can be collected in a relatively small volume of sediment. They are also ubiquitously distributed and highly diverse in marine sediments. Many studies have also shown that meiofauna are an important component in marine benthic ecosystems because of their small size, high abundance and fast turnover rates. They play an important role in marine benthic food chains. As the dominant meiofaunal group, nematodes have a direct development phase, with a short life-cycle of one to three months. Hence, changes in the community structure can be readily observed in short-term studies. The importance of using meiofauna as environmental indicators has been recognized in many ecological studies, especially when investigating the effects of anthropogenic activities. This is particularly true for nematodes. However, studies about the response of meiofauna in a community recovering from anthropogenic activities are very limited. Only a few such studies were reported in temperate waters, which showed that the recovery of a nematode community from organic pollution could be slow. Interestingly, a relatively faster recovery rate was noted after the physical disturbance of their sediment habitat. No published studies have been reported in tropical or subtropical waters to date. Whether or not tropical/subtropical meiofauna show a different or faster response because of climatic and latitudinal differences thus requires investigation. The aim of the present study is to examine the response of meiofauna, especially nematodes, upon recovery from anthropogenic activities in the subtropical waters of Hong Kong. The examination includes responses to the cessation of organic pollution from sewage discharges and physical disturbance from deployment of artificial reefs and the cessation of bottom trawling activities. In the past, Victoria Harbour had suffered from serious eutrophication from sewage discharges. Meiofauna and nematodes inhabited in Victoria Harbour, where water quality has been improved as the result of a large-scale sewage treatment project which was implemented in 2001, were studied in order to assess the changes in sediment quality. A three-year survey (from June 2004 to February 2007) was conducted by taking grab sediment samples in wet (summer) and dry (winter) seasons at two inside-harbour sites (Sai Wan Ho, Causeway Bay) and three outside-harbour sites (eastern side: Tung Lung Chau; western side: Tsing Yi, Peng Chau). In general, the benthic recovery process was assessed through investigations of: (1) physico-chemical parameters of sediments; (2) meiofaunal abundance and the main animal group composition; (3) nematode community structure and (4) biological traits analysis of nematode community. A field transplantation experiment and a laboratory microcosm experiment were also conducted to study the response of the nematode community upon the abatement of organic pollution using sediments from Victoria Harbour. In order to assess the response of meiofaunal and nematode communities to the deployment of artificial reefs and the cessation of bottom trawling activities, a one-year study (from April 2006 to January 2007) on the changes of the meiofaunal community was undertaken. Sediment samples were obtained using a 0.1 m2 van Veen grab, on a seasonal basis, from a Marine Protected Area (MPA) with the presence of artificial reefs and the absence of bottom trawling activities, as well as from its adjacent area with the absence of artificial reefs and the presence of bottom trawling activities in Outer Port Shelter, Hong Kong. In the Victoria Harbour study, the physico-chemical parameters of the sediments, including sediment median diameter (Md), total organic carbon (TOC), total Kjeldahl nitrogen (TKN) and total phosphorus (TP), were analyzed. Over the study period of three years, there was no significant improvement of the sediment physico-chemical parameters inside the harbour, where the sediment was organically polluted from sewage discharges prior to the implementation of the large-scale sewage treatment project. Away from the sewage disposal area, the outside-harbour sediments had relatively lower nutrient levels. The abundance of meiofauna and nematodes at the eastern outside-harbour site was significantly higher than those at the two inside-harbour sites. However, the abundance of meiofauna and nematodes at the western outside-harbour sites was not significantly higher than those at the inside-harbour sites. For temporal changes, the abundance of meiofauna and nematodes recorded in the last winter sampling of the study (February 2007), at the two inside-harbour sites, showed the highest values and were significantly different from the other five samplings. This suggested that the quality of the sediment habitat for meiofauna registered improvement after the cessation of sewage discharges, although it was not reflected from the sediment physico-chemical parameter analysis. A total of 188 species of free-living marine nematodes, belonging to five orders, 33 families and 118 genera, were identified in the Victoria Harbour study. Further examination of the nematode community, using multivariate statistical analyses, showed that there were distinct differences in community structure at the inside- and outside-harbour study sites. The dominant species number at the outside-harbour sites (five to 17 species) was higher than those at the inside-harbour sites (three to six species), indicating that the outside-harbour areas can support a much higher diversity of nematodes than the inside-harbour areas. There were four dominant species (Paradontophora sp., Sabtieria praedatrix, Terschellingia longicaudata, and Terschellingia communis) in most the inside- and outside-harbour site samples. The number of nematode species (S), Shannon-Wiener diversity index (H’) and Margalef’s species richness (d) at the eastern outside-harbour site were significantly higher than those at the inside-harbour sites. Conversely, similar biological indices at the western outside-harbour sites were not significantly different with the inside-harbour sites. Such a spatial difference between the inside- and outside-harbour sites was largely due to the poor sediment quality within the harbour over the years. Looking at the historical data, the sediments suffered from such high amounts of organic enrichment, that the total organic matter increased from 2-4% in 1977 to 3.6-7.5% in 2001; this was prior to the implementation of the large sewage treatment project. Additionally, the sediments were found to be contaminated with heavy metals and trace organics. There was a significant temporal variation for the nematode community at one of the inside-harbour sites, i.e., nematode community became similar to the western outside-harbour in the last sampling, close to the end of the three-year study. TKN was found to be the most important correlating factor of the grouping of the nematode communities in the study area. The change of the nematode community structure at the inside-harbour sites further confirmed the recovery process of sediment quality in Victoria Harbour. In addition, functional considerations and biological traits analysis (BTA) were used to investigate the response of the nematode community to the cessation of sewage discharges. Data showed that there was a recovery trend for a better benthic environment at the inside-harbour sites according to the trophic structure of the nematode community, the 1B/2A (non-selective deposit feeders and epigrowth feeders of nematodes) ratio and BTA, with additional information from nematode tail shape, adult body length and body shape. However, information supplied by the c-p (colonizer-persister) scale and maturity index (MI) of nematode community was not consistent with the above results. The present findings suggested that BTA, using a range of biological traits for the nematode species, can be a useful tool in monitoring the recovery of nematode communities during the abatement of organic pollution, while it should be carefully considered when using a single trait or index to monitor pollution. In order to further assess the recovery rate of the nematode community upon abatement of the organic pollution, a field transplantation experiment was conducted in Tai Tam, which is a non-polluted, shallow subtidal habitat on the south of Hong Kong Island, using sediments from the eastern outside-harbour site and one inside-harbour site, plus sediments from Tai Tam as the control. Fresh sediments with meiofauna were collected from the aforementioned sites, placed in plastic trays and transplanted to Tai Tam. Sediments were retrieved at the start of the experiment and at the 1-, 3-, and 8-week points after transplant for analysis of the nematode communities. Results showed that the nematode communities in the control sediments were consistent in the four sampling times, while it took three and eight weeks, respectively, for the nematode communities from the outside-harbour and inside-harbour sites to become similar with the control. This indicated that the relatively poor habitat quality and the nematode community composition in the organically polluted inside-harbour sediments required a longer time for recovery, as compared to the samples from the better habitat quality and the nematode community composition in the outside-harbour sediments. A two-month laboratory microcosm experiment was also conducted to study the response of nematode communities to the abatement of organic pollution, i.e., to compare nematode communities in sediments with different organic contents, which were manipulated by mixing defaunated sediment formed by defrosting a frozen sediment sample collected at an inside-harbour site with the same sediment, after the removal of organic matter through combustion. Five treatments were set up, including a positive control (defaunated sediment only), high, medium and low organic content treatments (mixing the positive and negative control sediments according to different ratios), and a negative control (combusted sediment only). The nematode communities from the fresh sediments obtained from the inside-harbour site and from the five treatments from the end of the experimental period were analyzed. Results showed that nematode abundance was the highest in the high organic content treatment. Multivariate statistical analyses showed that the nematode communities were divided into two groups (Group 1: positive and negative controls; Group 2: inside-harbour sediment, high, medium and low organic content treatments). However, no significant differences were found for S, H’ and d among the treatments. The present experiment suggested that nematodes could proliferate in sediments with high organic content, which can enhance their abundance. However, nematode communities were affected not only by organic enrichment but also by other pollutants in the sewage-contaminated sediments. In the Outer Port Shelter study, results showed that the levels of TOC and TKN, the abundances of total meiofauna and nematodes, were significantly lower in the MPA than those in its adjacent area. Correlation analysis revealed that the abundance of total meiofauna and nematodes had significantly positive correlations with the levels of TOC and TKN in sediments. The H’ and d of nematode community were found to be higher in MPA only at the beginning of the field study (i.e., April 2006). However, the numbers of dominant nematode species in the MPA were higher than those in the outside-MPA area, which indicated that more nematode species could coexist in the habitat created by the MPA with presence of artificial reefs and the cessation of bottom trawling. Multivariate statistical analysis indicated that there were distinct nematode communities in the MPA and its adjacent areas. Further analysis, using proportions of nematodes with five biological traits related to buccal morphology, tail shape, body size, body shape and life history strategy, showed that there was no significant difference for nematode trophic structure. Conversely, the proportions of nematodes with clavate tail shape, adult length between 2-4 mm, stout body shape and K-strategy life history were higher in the MPA, while those of nematodes with elongated/filiform or a conical tail shape, adult length <1 and 1-2 mm, slender body shape and r-strategy life history were higher in its adjacent area. In summary, nematode community structure tended to become more resilient, although there was a decrease in the overall abundance of nematodes with presence of artificial reefs and the cessation of bottom trawling activities. The dominant species number, as well as proportions of species with larger size, stout body shape and K-strategy life history, increased as compared to its adjacent area where bottom trawling is still in operation. According to the present findings, biological responses, as indicated by the changes in abundance and community structure of meiofauna and nematode, trophic structure and BTA of nematode community, are more sensitive in reflecting the changes in sediment quality upon cessation of sewage pollution in Victoria Harbour. The rate of such recovery, however, was found to be slow over the three-year study, even in subtropical waters where water temperature and productivity turnover are higher than that in temperate waters. The abundance of meiofauna could be enhanced by bottom trawling because such physical disturbance could increase nutrient levels in sediments. Nematode community structure changed significantly with the presence of artificial reefs and the cessation of bottom trawling activities. There was an increase in the abundance of nematodes with a larger-sized body, stout body shape and K-strategy life history, making the nematode community structure more resilient. In conclusion, the response of the nematode communities to physical disturbances from deployment of artificial reefs and the cessation of bottom trawling activities appeared to be faster and more prominent than after the cessation of sewage pollution.