Environ Sci Pollut Res DOI 10.1007/s11356-014-2615-3
RESEARCH ARTICLE
Do early colonization patterns of periphytic ciliate fauna reveal environmental quality status in coastal waters? Henglong Xu & Wei Zhang & Yong Jiang
Received: 3 December 2013 / Accepted: 30 January 2014 # Springer-Verlag Berlin Heidelberg 2014
Abstract The feasibility for developing a protocol to assess marine water quality based on early colonization features of periphytic ciliate fauna was studied in coastal waters of the Yellow Sea, northern China. The ciliate communities with 3– 28-day ages were collected monthly at four stations with a spatial gradient of environmental stress from August 2011 to July 2012. The spatial patterns of both early (3–7 days) and mature (>10 days) communities of the ciliates represented significant differences among the four stations, and were significantly correlated with environmental variables, especially nutrients and chemical oxygen demand (COD). Seven and eight dominant species were significantly correlated with nutrients or COD within the early and mature communities, respectively. The species richness indices were strongly correlated with nutrients, especially in mature communities. These findings suggest that it is possible to assess the status of water quality using early colonization features of periphytic ciliate fauna in coastal waters. Keywords Marine bioassessment . Environmental stress . Field community . Periphytic ciliate . Coastal waters
Introduction With increasing environmental stress, anthropogenic impacts, and the global decline in biodiversity, there is a pressing need for methods to assess environmental/ecological quality that are rapid, reliable, and cost-effective. Ciliated protozoa have increasingly been proved to have many advantages in Responsible editor: Philippe Garrigues H. Xu (*) : W. Zhang : Y. Jiang Department of Marine Ecology, Ocean University of China, Qingdao 266003, China e-mail:
[email protected]
community-based bioassessment of many aquatic ecosystems (Cairns and Henebry 1982; Xu et al. 2005; Jiang et al. 2007; Shi et al. 2012). With their short life cycle and delicate membranes, they may respond more rapidly to environmental changes than any metazoa (Coppellotti and Matarazzo 2000; Ismael and Dorgham 2003; Kchaou et al. 2009). Many species can tolerate extremes of environmental conditions and inhabit biotopes that are unfavorable to most macrofauna (Risse-Buhl and Küsel 2009). Thus, the protozoa have widely been used as useful bioindicator to assess water quality in many aquatic ecosystems (Morin et al. 2008, 2010; Xu et al. 2011a, b; Jiang et al. 2013a, b, c). Periphytic ciliates are a primary component of the periphytic microfauna and play an important role in the functioning of microbial food webs by mediating the flux of organic matter and energy from the plankton to the benthos in many aquatic ecosystems (Bryers and Characklis 1982; Eisenmann et al. 2001; Fischer et al. 2002; Dubber and Gray 2009; Kathol et al. 2009; Norf et al. 2009a, b). Because of easy sampling, relative immobility, increasing availability of user-friendly taxonomic references and standardized methodologies for temporal and spatial comparisons, the ciliates have widely been accepted as potential indicators to evaluate environmental stress and anthropogenic impacts in many aquatic environments, especially the freshwater environments (Jiang et al. 2007; Xu et al. 2011c, d). So far, there have been several studies on community patterns and colonization dynamics of marine periphytic ciliates (Railkin 1998; Strüder-Kypke 1999; Kralj et al. 2006; Xu et al. 2009a, 2012a, b; Zhang et al. 2013). Their feasibility to assess rapidly marine water quality status based on their ecological features of early colonization patterns, however, has received comparatively little attention (Norf et al. 2009a, b; Xu et al. 2012c; Zhang et al. 2012a, b). A 1-year baseline survey of periphytic ciliate colonization patterns was conducted using glass slide as an artificial substratum in coastal waters of the Yellow Sea, near Qingdao, northern
Environ Sci Pollut Res Fig. 1 Sampling stations in coastal waters of the Yellow Sea, near Qingdao, northern China. (A) Station A, heavily stressed area in Jiaozhou Bay, the pollution being mainly in the form of organic pollutants and nutrients from domestic sewage and industrial discharge from several rivers; (B) station B, moderately polluted area Jiaozhou Bay by minor discharges from a small river entering the bay; (C) station C, slightly polluted area near the mouth of Jiaozhou Bay and relatively distant from the rivers entering the bay; (D) station D, relatively clean area which was out of this bay and more distant from the river discharges
China from August 2011 to July 2012. Our aims of this study were: (1) to reveal spatial variations in the taxonomic composition and community structure of periphytic ciliate communities with different ages; (2) to demonstrate the relationships between
colonization patterns of periphytic ciliate fauna and the environmental variables; and (3) to determine the feasibility of developing a protocol for assessing water quality based on the early colonization features of periphytic ciliate fauna in coastal waters.
Table 1 Environmental variables monitored at the four sampling stations in coastal waters of the Yellow Sea, near Qingdao, northern China during the 1year cycle (August 2011–July 2012) (mean values for a total of 20 samples from each sampling station) Variables
Station A
Station B
Station C
Station D
T (°C) pH Sal (psu) DO (mg l−1) Tra (m) COD (mg l−1)
17.33±7.30 8.12±0.31 29.46±3.05 7.63±1.28 1.81±0.45 0.64±0.31
17.43±7.08 8.26±0.31 29.90±3.03 7.92±1.26 2.00±0.60 0.66±0.36
17.34±6.94 8.24±0.34 30.01±3.40 7.85±1.40 2.45±0.92 0.52±0.36
17.78±6.97 8.24±0.36 29.65±3.97 8.24±1.22 3.78±0.85 0.66±0.23
NO2-N (μmol l−1) NO3-N (μmol l−1) NH4-N (μmol l−1) SRP (μmol l−1)
3.25±1.74 38.72±10.92 9.91±2.18 1.13±0.90
3.42±4.44 29.43±9.79 7.76±1.87 0.79±0.44
1.61±1.08 18.26±5.68 6.06±1.60 0.51±0.31
2.54±3.21 24.02±7.77 6.70±2.47 0.72±0.41
T water temperature, Sal salinity, DO dissolved oxygen, COD chemical oxygen demand (COD), Tra transparency, SRP soluble active phosphate, NO3-N nitrate nitrogen, NO2-N nitrite nitrogen, NH4-N ammonium nitrogen
Environ Sci Pollut Res Table 2 List of periphytic ciliates recorded at the four sampling stations, including presence/absence (P/A) during 3-, 7-, 10-, 14-, and 28-day colonization periods, occurrence (%) and abundance (%) at each of the Species
Station A
four sampling stations in coastal waters of the Yellow Sea, near Qingdao, northern China during a 1-year cycle (August 2011–July 2012)
Station B
Station C
Station D
P/A
Occu
RA
P/A
Occu
RA
P/A
Occu
RA
P/A
Occu
RA
Aspidisca aculeata Pseudovorticella sp. Zoothamnium alternans Hartmannula angustipilosa Diophrys appendiculata Trochilia minuta Coeloperix sleighi Tachysoma ovata Orthodonella apohamatus Metaurostylopsis sp.1 Uronema marinum Pseudovorticella paracratera Hartmannula derouxi
+++++ +++++ +++++ +++++ +++++ +++++ +++++ +++++ +++++ +++++ +++++ +++++ +++++
87.18 84.62 79.49 69.23 61.54 58.97 58.97 58.97 56.41 53.85 51.28 51.28 48.72
1.13 3.36 48.67 0.25 0.24 6.52 0.03 0.92 0.05 0.15 0.16 0.70 0.15
+++++ +++++ +++++ +++++ +++−+ +++++ +++++ +++++ +++++ +++++ +++++ +++++ +++−+
89.19 83.78 54.05 64.86 62.16 29.73 54.05 59.46 40.54 48.65 48.65 54.05 35.14
3.05 17.78 2.84 2.13 0.60 0.89 0.22 1.59 0.70 0.39 0.17 19.88 0.06
+++++ +++++ +++++ +++++ +++++ −++++ +++−+ +++−+ +++−+ +++++ +++++ +++−+ +++−+
84.21 68.42 63.16 42.11 63.16 21.05 57.89 52.63 21.05 50.00 47.37 50.00 26.32
1.62 32.02 12.40 0.03 0.19 0.01 0.22 0.21 0.04 0.40 0.05 1.43 0.02
+++++ +++++ +++++ +++++ +++++ −++++ +++++ +++++ +++−+ +++++ +++++ +++++ +++++
87.18 89.74 53.85 69.23 87.18 17.95 64.10 69.23 41.03 48.72 41.03 66.67 43.59
1.70 65.71 2.27 0.60 1.24 0.01 0.46 0.52 0.21 0.57 0.45 3.18 0.21
Aspidisca steini Euplotes rariseta Litonotus paracygnus Dysteria pusilla Psammomitra retractilis Metaurostylopsis salina Loricophrya tuba Holosticha heterofoissneri Aspidisca magna Ephelota mammillata Acineta tuberosa Litonotus yinae Euplotes vannus
+++++ +++++ +++++ +++++ +++++ +++++ +++++ +++++ +++++ +++++ +++++ +++−+ +++−+
48.72 48.72 48.72 46.15 43.59 41.03 41.03 41.03 41.03 38.46 35.90 23.08 35.90
0.12 0.02 0.02 0.06 0.06 0.50 0.38 0.02 0.01 0.50 0.40 0.02 0.01
+++++ +++++ +++−+ +++++ +++++ +++++ +++−+ +++++ +++++ +++++ ++++− +++++ +++++
70.27 27.03 54.05 40.54 54.05 43.24 29.73 45.95 59.46 32.43 43.24 56.76 35.14
0.74 0.02 0.21 0.10 0.16 0.97 1.28 0.30 0.44 0.22 0.31 0.24 0.03
+++++ +++++ +++++ +++++ +++−+ +++++ +++−+ +++++ +++++ +++++ +++++ +++++ −++++
71.05 39.47 60.53 34.21 57.89 47.37 26.32 42.11 65.79 68.42 63.16 34.21 26.32
0.39 0.02 0.24 0.02 0.14 0.11 1.29 0.04 0.23 0.20 1.21 0.15
