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Colonization features of marine biofilm-dwelling protozoa in Chinese coastal waters of the Yellow Sea

  • Corresponding author: Henglong Xu, henglongxu@126.com
  • Received Date: 2020-02-14
    Accepted Date: 2020-03-24
    Published online: 2020-04-27
  • Edited by Chengchao Chen.
  • Colonization features of biofilm-dwelling protozoa, especially ciliates, are routinely used as a useful tool for marine bioassessment. In this review, we summarize some of these features to develop an optimal sampling strategy for using biofilm-dwelling protozoa as bioindicators of marine water quality. We focus on the utility of: (1) diversity indices to analyze the colonization features of biofilm-dwelling protozoa for monitoring marine water quality; (2) MacArthur-Wilson and logistic equation models to determine spatio-temporal variations in colonization dynamics; and (3) homogeneity in taxonomic breadth of biofilm-dwelling protozoa during the process of colonization. The main findings are that: (1) the colonization dynamics of biofilm-dwelling protozoa are similar at depths of 1-5 m in spring and autumn; (2) temporal variability was well fitted to the MacArthur-Wilson and logistic models (P < 0.05); and (3) species composition reached an equilibrium after a colonization period of 10-14 days in spring and autumn, but this took less time in the summer and more time in the winter. Ellipse-plotting tests demonstrated spatial variability in homogeneity in taxonomic structure of the ciliate communities at different depths in the water column, with high levels at 1 m and 2 m and lower levels at 3.5 m and 5 m. Thus, the findings of this review suggest that the colonization dynamics of biofilm-dwelling protozoa may be influenced by different depths and seasons in coastal waters and 1-2 m in spring and autumn may be optimal sampling strategy for bioassessment on large spatial/temporal scales in marine ecosystems.
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Colonization features of marine biofilm-dwelling protozoa in Chinese coastal waters of the Yellow Sea

    Corresponding author: Henglong Xu, henglongxu@126.com
  • 1. Laboratory of Microbial Ecology, Ocean University of China, Qingdao 266003, China
  • 2. Institute of Marine Sciences, University of Chittagong, Chittagong 4331, Bangladesh
  • 3. Department of Life Sciences, Natural History Museum, London SW7 5BD, UK

Abstract: Colonization features of biofilm-dwelling protozoa, especially ciliates, are routinely used as a useful tool for marine bioassessment. In this review, we summarize some of these features to develop an optimal sampling strategy for using biofilm-dwelling protozoa as bioindicators of marine water quality. We focus on the utility of: (1) diversity indices to analyze the colonization features of biofilm-dwelling protozoa for monitoring marine water quality; (2) MacArthur-Wilson and logistic equation models to determine spatio-temporal variations in colonization dynamics; and (3) homogeneity in taxonomic breadth of biofilm-dwelling protozoa during the process of colonization. The main findings are that: (1) the colonization dynamics of biofilm-dwelling protozoa are similar at depths of 1-5 m in spring and autumn; (2) temporal variability was well fitted to the MacArthur-Wilson and logistic models (P < 0.05); and (3) species composition reached an equilibrium after a colonization period of 10-14 days in spring and autumn, but this took less time in the summer and more time in the winter. Ellipse-plotting tests demonstrated spatial variability in homogeneity in taxonomic structure of the ciliate communities at different depths in the water column, with high levels at 1 m and 2 m and lower levels at 3.5 m and 5 m. Thus, the findings of this review suggest that the colonization dynamics of biofilm-dwelling protozoa may be influenced by different depths and seasons in coastal waters and 1-2 m in spring and autumn may be optimal sampling strategy for bioassessment on large spatial/temporal scales in marine ecosystems.

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Introduction
  • Ciliates are one of the most species-rich groups in the microeukaryotic periphyton community and are found in a variety of habitats in marine ecosystems (Bai et al. 2019; Guo et al. 2019; Lynn 2008; Sikder et al. 2019a, b, c; Sikder and Xu 2020; Xu et al. 2016). Foissner (1992) estimated that the number of free-living ciliate species is probably more than 40, 000 and that > 80% of these have yet to be described.

    Ciliates play an important role in the energy flux of aquatic ecosystems (Abdullah Al et al. 2018a; Jiang et al. 2012, 2013; Kathol et al. 2011; Madoni and Braghiroli 2007; Norf et al. 2007; Xu et al. 2016; Yang et al. 2016). Many are periphytic, closely allied with or being attaching to various substrata in the water column, especially at the interface between the bottom sediments and water (Sikder et al. 2019c; Xu et al. 2016; Zhang et al. 2012). These periphytic, or biofilm-dwelling, ciliates respond rapidly to environmental change in terms of their species richness and the heterogeneity of their community structure (Sikder et al. 2020; Xu et al. 2009a, 2016; Yang et al. 2004). Periphytic ciliates are widely used as bioindicators of the quality and ecological status of aquatic ecosystems due to their quick response to environmental fluctuations, ease of sampling and observation compared to any other microeukaryotic organisms (Foissner 1992; Foissner and Berger 1996; Kchaou et al. 2009; Liebmann 1951; Sikder and Xu 2020; Sladecek 1983; Xu and Xu 2016; Zhang et al. 2012, 2013).

    Coastal waters are subject to a wide range of environmental risks including pollution and climate change, the impacts of which are vigorously debated. It is generally acknowledged that global climate change and pollution are having a significant adverse effect on coastal ecosystems (Walther et al. 2002). Eutrophication, for example, can cause dramatic change in environment/ecological quality status, thereby reducing biodiversity and negatively impacting ecosystem function (Lotze et al. 2006; Villéger et al. 2010; Vitousek et al. 1997). Based mainly on recent reports by the Henglong Xu group at Ocean University of China (OUC), Qingdao (e.g., Sikder et al. 2019a, c : Sikder and Xu 2020; Zhang et al. 2012, 2013), this paper reviews the colonization features of biofilm-dwelling ciliates and other protozoa to determine the optimal sampling strategy for bioassessment of marine coastal ecosystems.

  • General features of colonization dynamics

  • Traditional biodiversity indices, for example, species richness, evenness and diversity along with functional parameters, e.g., colonization rate constant, are commonly employed in aquatic community investigations (Connell 1978; Magurran 1991; Tan et al. 2010). To use these indices for bioindication and tracking the consequence of pollution on the biotic components, it is necessary to know the process of colonization and specific community structure. Most studies have focused on freshwater ecosystems; whereas, the colonization dynamics of marine biofilm-dwelling ciliates is poorly investigated (Mieczan 2010; Xu et al. 2002, 2005; Zhang et al. 2012). Additionally, little information is available on seasonal variations of ciliate colonization or the optimal depth in the water column for determining periphytic ciliate community structure (Coppellotti and Matarazzo 2000; Gong et al. 2005).

    According to previous reports, microeukaryotic organisms commonly follow the MacArthur-Wilson equilibrium model in terms of species number and the logistic growth equation for numbers of individuals during the process of colonization (Cairns and Henebry 1982; MacArthur and Wilson 1967; Railkin 1995). The colonization process can be divided into three separate phases: initial (1-7 days old), transitional (7-10 days old) and equilibrium (10-28 days old) (Burkvoskii et al. 2011; Burkovskii and Mazei 2001; Sonntag et al. 2006). It was previously reported that the value of Seq (estimated equilibrium of species number) is generally negatively correlated with concentrations of organic pollutants and toxic compounds; while, the value of G (colonization rate constant) is generally higher in waters with lower environmental stress (Burkvoskii et al. 2011; Burkovskii and Mazei 2001; Cairns and Henebry 1982; Xu et al. 2009b). To verify the above conclusions, Zhang et al. (2013) applied the MacArthur-Wilson equilibrium and logistic growth equation models to periphytic ciliate communities in northern Chinese coastal regions of the Yellow Sea. In terms of species composition (i.e., presence/absence matrices), communities of biofilm-dwelling ciliates and other protozoa showed significantly high similarities during the equilibrium stages, but clearly differed from initial- and exponential-stage communities. This means the periphytic ciliate community structure changes significantly during the 28-day colonization period reaching equilibrium in species composition within at least 10 days (Fig. 1a-d; Zhang et al. 2013). Similar results were reported by Norf et al. (2007) and Xu et al. (2005). It was noted that, however, periphytic ciliate communities showed no significant differences in functional patterns with depth; the species numbers and colonization rates of heterotrophic functional groups were significantly higher at 1 m than in deeper layers. This may be due to the decrease in sunlight and food supplies at deeper layers in the water column. These factors may also account for the higher accumulative species number and individual abundance at 1 m compared to the deeper layers. Furthermore, the colonization curves and the increase in abundance of biofilm-dwelling ciliates and other protozoa closely fitted the MacArthur-Wilson model, and a logistic equation showed differences in functional parameters, i.e., Seq, G and T90%, representing equilibrium species numbers, colonization rates and the time to 90% Seq, respectively, among different depths in the water column (Fig. 1a-h; Sikder et al. 2019a).

    Figure 1.  Colonization curves and growth curves of biofilm-dwelling protozoa at four depths in coastal waters of the Yellow Sea, northern China during a 4-season period.Adapted from figures of (Sikder et al. 2019a). Colonization curves, a, 1 m (initial at days 3-7; transition at days 7-10; equilibrium at days 14-28); b, 2 m and c, 3.5 m (initial at day 3; transition at days 7-14; equilibrium at days 21-28); d, 5 m (non-uniform colonization). Growth curves, e, 1 m; f, 2 m, g, 3.5 m; h, 5 m

    Using glass microscope slides as artificial substrates, Zhang et al. (2012) demonstrated that abundances of trophic-functional groups (i.e., algivores, bacterivores, photoautotrophs, saprotrophs) were higher than raptors in shallower layers than in deeper layers. This implies that initially, bacteria colonize the slide surface, followed by autotrophic flagellates and diatoms; the next groups are vagile species of amoebae, ciliates and bacterivorous, finally larger species along with sessile feeders and broader feeding spectrum appear. These findings are consistent with those from other aquatic ecosystems (Railkin 1995). It should be noted that the classic MacArthur-Wilson model does not cover only a saturation curve of accumulated species number; somewhat, it also supposes that the number of species is fixed by a dynamic equilibrium between immigration and extinction.

    Previous studies have shown that benthic and planktonic resource groups both play a key role in shaping the functional structure of biofilm-dwelling ciliates and other protozoan communities (Früh et al. 2011; Kathol et al. 2011; Norf and Weitere 2010). Heterotrophic consumers in biofilms, for example, are often dominated by planktivorous groups (suspension feeding), such as peritrichs, rather than periphytivores or benthivores (Kathol et al. 2011). Consequently, the functional groups of benthic consumers should be further categorized by their food preferences when exploring either their role in responses to enrichment with bacteria/ algae or controlling the composition of the periphyton and plankton. Zhang et al(2012, 2013), thus, provide important findings for ecological research and monitoring programs using communities of marine periphytic ciliates and other protozoa at different stages of colonization.

    Biodiversity measures have a number of limitations for quantifying environmental changes due to the restrictions of their dependence on sampling effort or sample size (Prato et al. 2009; Warwick and Clarke 2001). Otherwise, they are not easy to link with environmental data since their relationships remain controversial and are not always monotonic, especially when comparing data collected by methods that are not standardized in terms of procedure or sample size (Prato et al. 2009). Furthermore, there is no statistical framework for testing whether the values of these parameters are higher or lower than expected for a given location or region (Clarke and Warwick 1998; Prato et al. 2009). The studies by Zhang et al(2012, 2013), for example, were conducted based on one dataset for coastal waters at a single location (Yellow Sea coast of northern China) collected in a single season (summer). Thus, further studies on a range of marine habitats carried out over extended times are necessary to confirm the above findings.

  • Seasonal pattern of colonization dynamics

  • Some studies on community structures and community patterns of marine ciliates and other protozoa have been conducted (Duong et al. 2007; Gong et al. 2005; Railkin 1995; Xu et al. 2012a, b; Zhang et al. 2013). Few studies, however, have investigated seasonal variations of their colonization dynamics, although such data are important to both biomonitoring programs and microbial ecological research (Xu et al. 2012b; Zhang et al. 2015).

    Sikder and Xu (2020) investigated the seasonal colonization processes of periphytic ciliates at 1 m depth in Chinese coastal waters of the Yellow Sea. They noted different temporal dynamics among the four seasons during a 12-month period although all were well fitted to the MacArthur-Wilson equilibrium and the logistic models (Fig. 2a-h). The colonization dynamics of the periphytic protozoa, for example, were similar in the spring and autumn (Seq = 29/23; G = 0.301/0.296; T90% = 7.650/7.779) differed significantly in the summer and winter (Seq = 32/121; G = 0.708/0.005; T90% = 3.252/479.705). This was probably due to differences in the water conditions (e.g., water temperature) and food supply among the four seasons as stated by Abdullah Al et al. (2019) and Zhang et al. (2015). Otherwise, these findings provide clear evidence that the colonization process of periphytic ciliates and other protozoa may differ under different seasonal conditions. Distance-based redundancy analysis ordinations (dbRDA) showed that the process of colonization at 1 m depth was clearly classified into three separate phases among the four seasons (Fig. 4). Previously similar findings were reported by Bamforth (1982), Mieczan (2010) and Zhang et al(2012, 2013). Conversely, both PERMANOVA and SIMPROF tests revealed noteworthy differences in different colonization stages among the four seasons (Figs. 3, 4, 5). Hence, these findings recommend that different sampling strategies for different seasons are necessary in monitoring programs of marine ecosystems.

    Figure 2.  Colonization curves and growth curves of biofilm-dwelling protozoa in four seasons in coastal waters of the Yellow Sea, northern China during a 4-season period. Adapted from figures of (Sikder and Xu 2020). Colonization curves, a, spring (initial stage days 3-7; transition stage days 7-10; equilibrium stage days 14-28); b, summer (non-uniform colonization) and c, autumn (initial stage day 3; transition stage days 7-14; equilibrium stage days 21-28); d, winter (non-uniform colonization). Growth curves, e, spring; f, summer; g, autumn; h, winter

    Figure 3.  Cluster analyses with SIMPROF tests: showing significant variation in colonization stages of biofilm-dwelling protozoa during a 4-season period in coastal waters of the Yellow Sea, northern China. Adapted from figures of (Sikder and Xu 2020). a, spring; b, summer; c, autumn; d, winter

    Figure 4.  Distance-based redundancy analyses: showing the seasonal variations in community structure of periphytic protozoa during the colonization process in coastal waters of the Yellow Sea, northern China, during a 4-season period. Adapted from figures of (Sikder and Xu 2020). Ordinations: a, spring; b, summer; c, autumn; d, winter

    Figure 5.  Cluster analyses with SIMPROF tests: showing significant variation in each of the colonization stage of periphytic ciliates at each depth within colonization process during a 4-season period in coastal waters of the Yellow Sea, northern China. Adapted from figures of (Sikder et al 2019a). a 1 m; b, 2 m; c, 3.5 m; d, 5 m

  • Vertical variation in colonization dynamics

  • Periphytic ciliates utilize a variety of food supplies (e.g., algae/bacteria/detritus, etc.), the bases of which are generally planktonic in origin (Wang and Xu 2015; Weitere et al. 2003). The colonization processes of marine periphytic ciliates can, therefore, be shaped by the response of their food supply to changes in environmental conditions (e.g., sunlight, microalgae and nutrients) at different depths in water column (Abdullah Al et al. 2018b; Xu et al. 2009a, b; Zhang et al. 2013). Even though some investigations on the colonization processes of marine periphyton communities have been carried out, few of these have focused on their vertical variation in the water column. It has previously been reported that marine periphyton, especially ciliate communities, exhibit clear temporal and spatial succession throughout colonization of artificial substrates, particularly with relation to food supply, light intensity and nutrients (Li et al. 2009; Xu et al. 2009a, b; Xu et al. 2014a, b). These studies were, however, largely limited to surface waters, i.e., the uppermost 1 m of the water column. To use colonization dynamics of periphytic ciliates as pollution bioindicators, it is necessary to determine the optimal depth in the water column for community and ecological research.

    Sikder et al. (2019a) reported that patterns of colonization dynamics by marine periphytic ciliates differed among four water depths. The colonization dynamics of the ciliates fitted the MacArthur-Wilson and logistic equation models at different depths (i.e., 1 m, 2 m and 3.5 m) and the projected maximum values of abundances denoted a declining tendency from a depth of 1 m-5 m (Fig. 1a-h). This suggests that colonization by periphytic ciliate communities is influenced by variations in food supply that, in turn, is correlated with physical-chemical conditions, e.g., sunlight, nutrients, etc., at different depths in the water column. Using distance-based redundancy analysis ordinations, Sikder et al. (2019a) demonstrated that the colonization process at 1 m depth occurs in three separate stages (Fig. 6) which is consistent with earlier reports such as Bamforth (1982), Mieczan (2010), Xu et al.(2009a, b), and Zhang et al(2012, 2013). Conversely, PERMANOVA tests revealed significant differences in the patterns of colonization at each of four depths in the water column (Fig. 6). Sikder et al. (2019a) also observed that the colonization rate (G), equilibrium species number (Seq, ) and carrying capacity (Nmax) showed vertical variability from depths of 1-5 m in the water column. The highest values of each were measured at 1 m depth; while, lower values were found at 2 m, 3.5 m and 5 m (Fig. 1a-d). Nevertheless, these measures/parameters levelled off at a depth of 1-3.5 m (Fig. 1a-c) suggesting that lower light intensity in deeper water depths might influence the availability of food supply and, therefore, the periphytic ciliate colonization process. Sikder et al. (2019a), thus, represents an important reference for adopting an ideal sampling plan for bioassessment using marine periphytic ciliates. In the case of Chinese coastal waters of the Yellow Sea, 1 m appears to be the optimal depth for sampling periphytic ciliate communities.

    Figure 6.  Distance-based redundancy analyses: showing vertical variation in community structure of periphytic protozoa within the colonization process in coastal waters of the Yellow Sea, northern China during a 4-season period. Adapted from figures of (Sikder et al. 2019a). Ordinations: a, 1 m; b, 2 m; c, 3.5 m; d, 5 m. Vectors: e, 1 m; f, 2 m; g, 3.5 m; h, 5 m

  • Taxonomic breadth and the colonization process

  • Taxonomic distinctness is a key of biodiversity used to identify the average taxonomic relatedness between species/members in a community (e.g., Clarke and Warwick 1998). It is based largely on the taxonomic order of members of each species pair and after that averaging their relatedness crosswise entire species pairs while branch sizes are totally unidentified. A foremost advantage of this key is its individuality of sampling frame/effort (e.g., Magurran 2003). Several investigations have concluded that the distribution of taxonomic relatedness is an effective way of defining the withdrawal of community pattern from an expected taxonomic structure caused by environmental pressure (Arvanitidis et al. 2009; Jiang et al. 2012; Warwick and Clarke 2001). Thus, taxonomic distinctness has routinely been used as a powerful bioindicator both in ecological research and in monitoring programs of environmental quality (Xu et al. 2015, 2016; Yang et al. 2016; Zhao et al. 2016).

    Sikder et al. (2019c) used taxonomic breadth to study the colonization dynamics of biofilm-dwelling protozoa in coastal ecosystems. It was noted that these protozoa are subject to significant variability in taxonomic structure both temporally, i.e., before reaching the equilibrium phase, and vertically in the water column. Specifically, the homogeneity in taxonomic breadth was less in young communities (< 10 days old) and abundant in mature samples (> 10 days old) at the four water depths. This indicates that the taxonomic structure of the ciliate and other protozoan communities may considerably alter during the process of colonization.

    Benefits of taxonomic distinctness measures for investigating changes in members of each community patterns comprise their low sensitivity to sampling frame/effort and sample size and their usefulness for testing the consequence of departure from anticipation within a statistical outline (Clarke and Warwick 1998; Prato et al. 2009; Somerfield et al. 2008). In their report, Sikder et al. (2019c) used ellipse-plotting tests on the paired measures Δ+ and Λ+, i.e., average taxonomic distinctness and variation in taxonomic distinctness. These showed a vertical difference in similarity in taxonomic breadth of ciliate and other periphytic protozoan communities from a depth of 1-5 m, with higher levels at 1-2 m compared to those at 3.5-5 m (Fig. 7). These results suggest that Δ+ and Λ+ may be used for determining homogeneity in taxonomic breadth of periphytic protozoan communities during the colonization process.

    Figure 7.  Ellipse plots of 95% probability regions with a range of sub-list sizes of 10 and 20 for the pairs of average taxonomic distinctness (Δ+) and variation in taxonomic distinctness (Λ+) of periphytic ciliates at four water depths in coastal waters of the Yellow Sea, northern China. Adapted from figures of (Sikder et al. 2019c). a 1 m; b, 2 m; c, 3.5 m; d, 5 m

Conclusion
  • Here, we have reviewed the colonization features of biofilm-dwelling protozoa and their utility as robust bioindicators of marine water quality. It has been demonstrated that in Chinese coastal waters of the Yellow Sea, the colonization dynamics of biofilm-dwelling protozoa are similar at depths of 1-3.5 m in spring and autumn and that their temporal variability was well fitted to the MacArthur-Wilson and logistic models (P < 0.05). Furthermore, species composition reached an equilibrium after a colonization period of 10-14 days in spring and autumn, but this took less time in summer and more time in winter. By contrast, functional parameters, e.g., Seq, G and T90%, representing equilibrium species numbers, colonization rates and the time to 90% Seq, respectively, showed a clear seasonal variability. Moreover, ellipse-plotting tests established a spatial variability in similarity in taxonomic structure of the periphytic protozoan communities at depths of 1-5 m in the water column, with higher levels at 1 and 2 m compared to those at 3.5 and 5 m. Thus, the findings of this review suggest that the colonization dynamics of biofilm-dwelling protozoa may be influenced by different depths and seasons in coastal waters and 1-2 m in spring and autumn may be optimal sampling strategy for bioassessment on large spatial/temporal scales in marine ecosystems.

    Finally, these studies show that the colonization features of biofilm-dwelling protozoa differed with depth in the water column and seasonally, suggesting that an optimal sampling strategy needs to be developed for using colonization features of periphytic protozoa as bioindicators on marine water quality. It is noteworthy, however, that the studies of the Xu group were carried out on a relatively small area, i.e., northern Chinese coastal waters of the Yellow Sea, and hereafter, the dataset used for the modeling approach might not be applicable for other marine ecosystems around the world. Thus, further studies, on a range of aquatic environmental types, in different climatic regions, and over extended times are necessary for modeling environmental status using periphytic protozoa.

    Acknowledgements This work was supported by The Natural Science Foundation of China (Project Nos. 31672308, 41076089), and funded by the Research Group Project No. RGP-VPP-083, King Saud University Deanship of Scientifc Research. We thank Prof. Weibo Song, Laboratory of Protozoology, Ocean University of China (OUC), China, for his helpful discussions, Mr. Xinpeng Fan, Ms. Jiamei Jiang and Xumiao Chen, Laboratory of Protozoology, OUC, China, for their help with sampling and sample processing.

    Author contributions All authors wrote the paper and approved the fnal manuscript.

Compliance with ethical standards
  • Conflicts of interest The authors declare that they have no conficts of interest.

    Animal and human rights statement No human or animal subjects were used during the course of this research.

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