Environ Sci Pollut Res
DOI 10.1007/s11356-013-1525-0
RESEARCH ARTICLE
Functional groups of marine ciliated protozoa
and their relationships to water quality
Yong Jiang & Henglong Xu & Xiaozhong Hu &
Alan Warren & Weibo Song
Received: 28 November 2012 / Accepted: 25 January 2013
# Springer-Verlag Berlin Heidelberg 2013
Abstract Ciliated protozoa (ciliates) play important ecological roles in coastal waters, especially regarding their interaction with environmental parameters. In order to increase our
knowledge and understanding on the functional structure of
ciliate communities and their relationships to environmental
conditions in marine ecosystems, a 12-month study was carried out in a semi-enclosed bay in northern China. Samples
were collected biweekly at five sampling stations with differing levels of pollution/eutrophication, giving a total of 120
samples. Thirteen functional groups of ciliates (A–M) were
defined based on their specific spatio-temporal distribution
and relationships to physico-chemical parameters. Six of these
groups (H–M) were the primary contributors to the ciliate
communities in the polluted/eutrophic areas, whereas the other seven groups (A–G) dominated the communities in less
polluted areas. Six groups (A, D, G, H, I and K) dominated
during the warm seasons (summer and autumn), with the other
seven (B, C, E, F, J, L and M) dominating in the cold seasons
(spring and winter). Of these, groups B (mainly aloricate
ciliates), I (aloricate ciliates) and L (mainly loricate tintinnids)
were the primary contributors to the communities. It was also
shown that aloricate ciliates and tintinnids represented different
roles in structuring and functioning of the communities. The
results suggest that the ciliate communities may be constructed
Responsible editor: Philippe Garrigues
Co-first author (Y. Jiang & H. Xu)
Y. Jiang : H. Xu : X. Hu : W. Song (*)
Laboratory of Protozoology, Institute of Evolution and Marine
Biodiversity, Ocean University of China, Qingdao 266003, China
e-mail: [email protected]
A. Warren
Department of Zoology, The Natural History Museum,
Cromwell Road,
London SW7 5BD, UK
by several functional groups in response to the environmental
conditions. Thus, we conclude that these functional groups
might be potentially useful bioindicators for bioassessment
and conservation in marine habitats.
Keywords Ciliated protozoa . Environmental conditions .
Functional groups . Marine bioassessment . Spatio-temporal
distribution
Introduction
In aquatic environments, ciliated protozoa (ciliate) assemblages are an important component of the microplankton fauna
and are considered primary mediators of energy transfer from
pico- and nanoplankton production to higher trophic levels in
the functioning microbial loop (Dolan and Coats 1990;
Stoecker and McDowell-Cappuzzo 1990; Sime-Ngando et
al. 1995; Jiang et al. 2013). It is becoming increasingly recognised that there are several advantages in using ciliates for
the assessment of water quality. With their short life cycles and
delicate external membranes, they may react more rapidly to
environmental changes than many other eukaryotic organisms. Furthermore, many forms can inhabit environments that
are unfavourable to metazoans (Cairns et al. 1972; Franco et
al. 1998; Corliss 2002; Madoni and Braghiroli 2007; Jiang et
al. 2007). While most previous studies have focused on freshwater habitats, recent studies suggest that ciliates may also be
useful indicators of marine water quality (Kchaou et al. 2009;
Jiang et al. 2011a, b, 2012a, b; Xu et al. 2011a, b, c, d, e,
2012a, b, c, 2013; Zhang et al. 2012a, b, 2013).
Functional groups are defined as assemblages of species
with similar responses to a given environmental conditions or
a fixed habitat (Lavorel et al. 1998; Reynolds et al. 2002;
Mieleitner and Reichert 2008). For example, functional groups
of phytoplankton fauna have been established based on the
Environ Sci Pollut Res
Fig. 1 Sampling stations of
ciliated protozoa located in
Jiaozhou Bay, northern China.
A, station A near Huangdao;
B, station B near the mouths of
Yang and Dagu rivers; C,
station C near mariculture area;
D, station D near the mouths of
Haipo and Licun rivers; E,
station E at the mouth linking
Jiaozhou Bay with the Yellow
Sea
specific spatio-temporal ecological features with environmental
sensitivities and tolerances (Reynolds 1999; Padisák et al.
2009). The investigations using this system have provided
important information for understanding the dynamics of pelagic freshwater algal communities, especially for assessing the
water quality (Huszar et al. 2003; Padisák et al. 2006; Crossetti
and Bicudo 2008; Becker et al. 2009, 2010). However, there
have been few studies using functional groups of zooplankton
in marine environments (Sun et al. 2010).
In the present study, the functional structures of ciliate
communities were studied based on a 12-month dataset collected from Jiaozhou Bay, northern China (June 2007–May
2008). The main purpose is to identify functional groups of
ciliates, thereby addressing the following questions: (1) how
Fig. 2 Species distribution pattern of 62 planktonic ciliate protozoa in
1-yearcycle at five stations, including nine assemblages (a) and seven
sub-assemblages from assemblage I (b), plotted using group average
clustering on Bray–Curtis similarities from log-transformed species
abundance data. I–IX, assemblage I–IX; I1–I7, sub-assemblage I1–I7
Environ Sci Pollut Res
many functional groups of ciliates are there, (2) what are the
spatio-temporal distribution features that determine these
groups and (3) are these groups associated with specific
environmental conditions?
This study was conducted during June 2007 to May 2008 in
Jiaozhou Bay. Five sampling stations with differing levels of
pollution/eutrophication were selected (Fig. 1) (Jiang et al.
2011a, b). The sampling and fixation strategy, enumeration
and identification of ciliates and measurement of environmental
parameters followed that described by Jiang et al. (2012a, b).
Material and methods
Data analyses
Study area and data collection
Jiaozhou Bay is a semi-enclosed basin of the Yellow Sea,
northern China, with an area of 390 km2 and an average
depth of about 7 m. It is surrounded by the city of Qingdao
and connected the Yellow Sea via a narrow opening about
2.5 km wide.
Multivariate analyses were carried out using the PRIMER
v6.1 statistical package (Clarke and Gorley 2006). The
groups of ciliate communities were assigned by the routine
CLUSTER on Bray–Curtis similarities from fourth roottransformed species abundance data, while the differences
between groups were tested by the submodule ANOSIM
Fig. 3 Spatio-temporal variations in abundances (ind. per litre) of the nine assemblages (I–IX) in 1-yearcycle at five stations
Environ Sci Pollut Res
(Clarke and Gorley 2006). The spatial and temporal changes
of environmental status during the sampling period of the
five stations were both summarised using principal component analysis based on log–transformed/normalised abiotic
data (Clarke and Gorley 2006).
Results
Spatio-temporal species distribution
A total of 62 planktonic ciliate species were recorded, comprising 23 loricate forms (tintinnids) and 39 aloricate forms
(mainly oligotrichids). Dendogram of the species distribution
was plotted using group average clustering on Bray–Curtis
similarities from fourth root-transformed species abundance
data from the five sampling stations (Fig. 2). The clustering
analysis resulted in the 62 species falling into nine groups
(I–IX) at a 20 % similarity level. Group I was composed of 22
common/dominant species, mostly aloricate, with high occurrence/abundance and represented the primary contributors to
the ciliate communities (Fig. 2a, b). This group could be
further divided into seven subgroups (I1–I7) at a 45 % similarity level (Fig. 2b). Groups II–V, VII and VIII represented
assemblages of opportunistic loricate forms, mostly tintinnids, with low occurrence or abundance. Groups VI and
IX comprised rare species only (Fig. 2a). The analysis of
similarities revealed significant differences among the nine
groups (R=0.896, P=0.001) and the seven subgroups of
group I (R=0.835, P=0.001).
Fig. 4 Spatio-temporal variations in abundances (ind. per litre) of the seven sub-assemblages (I1–I7) from assemblage I in 1-yearcycle at five
stations
Environ Sci Pollut Res
Identification and succession dynamics of functional groups
The spatio-temporal variations of the nine ciliate groups and
the seven subgroups of group I are summarised in Figs. 3
and 4. It should be noted that those groups/subgroups occurred in specific spatio-temporal distribution patterns. For
instance, in July and August, group III mainly dominated
the communities at stations C and D (Fig. 3c), while subgroup I5 was dominant at station E (Fig. 4e). By contrast,
group I was represented throughout the 12-month period at
all stations but with only one major peak, i.e. at station E in
August, due to the contribution of subgroup I5.
A total of 13 functional groups (A–M) were recovered
based on the clustering analyses (Table 1); e.g. group B,
comprising group V and subgroup I5, mainly occurred at
station E in autumn (Figs. 3e and 4e, Table 1). Group I, mainly
comprising members of subgroup I4, occurred at station D in
spring and autumn (Fig. 4d, Table 1), and group L which
mainly comprised members of assemblage III, at stations C
and D in autumn (Fig. 3c, Table 1). Six groups (A, D, G, H, I
and K) comprised species that mainly occurred in summer and
autumn, whereas the other seven (B, C, E, F, J, L and M)
comprised species that mostly distributed in spring and winter.
Of these, groups B (mainly aloricate species, e.g. Mesodinium
pupula and Pseudotontonia cornuta), I (aloricate species, e.g.
Strombidium globosaneum, Strombidium capitatum and
Rimostrombidium veniliae) and L (mainly loricate tintinnids,
e.g. Tintinnopsis tocantinensis, Tintinnopsis orientalis and
Leprotintinnus bottnicus) were the primary contributors to
the communities. Otherwise, the aloricate ciliates and tintinnids represented different roles in structuring and functioning
of the ciliate communities.
The temporal variations in abundance of the 13 functional groups are shown in Fig. 5. In general, each functional
Table 1 Classification, composition, taxonomic characters,
seasonal 1 occurrence and
location of functional groups
of ciliated protozoa collected at
five stations in Jiaozhou Bay
during the study period
group peaked in specific time periods during the 12-month
cycle. However, it should be noted that some groups (e.g. C,
D, I and M) peaked during more than one season, whereas
the others (e.g. B, E, F and L) were confined to one season
only (Fig. 5).
Groups A–M showed a clear temporal variation in terms of
relative species number during the period of study, i.e. group I
(mainly aloricate species) was the primary contributor to the
communities, whereas groups B (mainly aloricate species and
some tintinnids) and L (mainly loricate tintinnids) only occurred during late summer and autumn (Fig. 6a). The variations in relative abundance showed similar temporal patterns,
i.e. group I was primarily responsible for the communities,
whereas groups B and L dominated the communities in late
summer and autumn in combination with group I (Fig. 6b).
Relationships between functional groups and environmental
variables
The results of the principal component analysis, with vectors
for spatio-temporal variations of both physical–chemical variables and functional groups of ciliates, are shown in Fig. 7. In
terms of temporal ordination, the analysis using nine abiotic
variables explained 67.5 % of the total temporal environmental
variability on the first two principal components (PC1 =53 %;
PC2 =14.5 %) and basically grouped the 12 months into the
four season (Fig. 7a). In the spatial ordination, the two principal
components accounted for 74.7 % of the total spatial environmental variability (PC1 =45.7 %; PC2 =29.0 %). The first axis
represented nutrients (e.g. NO3–N and NH3–N), thus separating the two less polluted stations (A and E) from the three more
polluted stations (B, C and D). The second axis, which represented salinity, Chl a, pH and SRP, separated station E from
station A, and station D from stations B and C (Fig. 7b).
Functional group
Composition
Taxonomic character
Season
Station
A
C
I7
VI
I5
V
I2
Non-loricate
Non-loricate
Non-loricate
Tintinnids
Non-loricate
Spring
Spring
Autumn
Autumn
Summer, winter
E
E
E
E
E
D
E
F
G
H
I
J
K
L
M
II
IV
I6
VIII
I3
I4
VII
IX
III
I1
Tintinnids
Tintinnids
Non-loricate
Tintinnids
Non-loricate
Non-loricate
Tintinnids
Non-loricate
Tintinnids
Non-loricate
Spring, winter
Summer
Summer
Autumn, winter
Spring
Spring, autumn
Autumn
Winter, spring
Autumn
Summer, autumn
A, E
A, E
A
A
D
D
D
C, D
C, D
B
B
species
species
species
species
species
species
species
species
species
Environ Sci Pollut Res
Fig. 6 Annual variations in relative species number (a) and relative
abundance (b) of the functional groups of ciliates (I–M) in Jiaozhou
Bay, northern China, during the study period
Fig. 5 Annual succession of the 13 ciliate functional groups (I–M) as a
function of abundance (ind. per litre) during the study period
Seven functional groups (A–G) dominated the ciliate
communities in the less polluted areas, whereas the other
six functional groups (H–M) were the primary contributors
to the communities in the more polluted/eutrophic areas.
Otherwise, six functional groups (A, D, G, H, I and K)
comprised species that occurred mainly in the cold seasons
(spring and winter), whereas the other seven (B, C, E, F, J, L
and M) comprised species that occurred mainly in the warm
seasons (summer and autumn).
Discussion
A number of studies have demonstrated that the ecological
patterns of ciliates are significantly related to environmental
conditions in a range of aquatic environments (Beaver and
Crisman 1982, 1989; Finlay and Esteban 1998; Jiang et al.
2007; Madoni and Braghiroli 2007; Kchaou et al. 2009; Jiang
et al. 2011a, b, 2012a, b; Xu et al. 2011a, b, c, d, e, 2012a, b, c,
2013; Zhang et al. 2012a, b, 2013). Although the importance
of functional groups of ciliates from marine ecosystems has not
been well recognised, especially with respect to the potential
capability in the assessment of water quality, our previous
investigations have revealed that spatio-temporal patterns of
ciliate communities are significantly correlated with environmental conditions and that some dominant species are significantly correlated with concentrations of nutrients (Jiang et al.
2011a, b, 2012a, b; Xu et al. 2011a, c). Thus, we hypothesise
that some ciliate assemblages, as functional groups with specific functional role in communities, could respond predictably
to different environmental conditions.
Defining functional groups of organisms for the purpose of
assessing environmental conditions or monitoring environmental change is often problematic. Reynolds (1980), for
example, defined 14 different groups of planktonic freshwater
algae in his scheme for assessing water quality. Subsequently,
some of these groups were sub-divided, and others were
added, doubling the total number of groups (Reynolds et al.
2002). The application of multivariate techniques has helped
to identify and validate such functional groups (Fabbro and
Duivenvoorden 2000; Kruk et al. 2002; Reynolds et al. 2002).
Environ Sci Pollut Res
Fig. 7 Principal component analysis plots based on log-transformed abiotic data of 12 months (a) and five stations (b)
In the present study, based on the specific spatio-temporal
patterns and the relationships to the environmental conditions,
a total of 13 functional groups of ciliates were identified using
a range of multivariate analyses. These functional groups displayed clear temporal successions with different groups dominating during different seasons (e.g. groups A, D, H and I for
vernal blooms, the B and L for associations at the start of
autumn). Furthermore, the functional groups also displayed
spatial preferences with different groups associated with different sampling stations according to the prevailing environmental conditions. Thus, the 13 groups could be ranked A to M
according to their occurrence at each sampling station in the
order from cleanest environmental conditions (stations E and
A) to more and more polluted ones (from station D to C and B).
The spatio-temporal characters and habitats of functional
Table 2 Habitat and tolerances/
sensitivities of functional groups
of 1 ciliated protozoa collected
at five stations in Jiaozhou Bay
during the study period
groups were summarised in Table 2, in order to provide a
potential useful reference to carry out functional group study
for characterising and understanding the spatio-temporal pattern of ciliate fauna in marine ecosystems. As indicated, in
single or coexist, the groups dominate the communities belonging to specific waters with fixed environmental conditions.
It was also shown that each group was possessed of its own
attribute, for instance, group B, which tended to dominate
under conditions of high water temperature and low salinity,
whereas group L was more tolerant of high organic pollutants,
especially such as those that occur in highly eutrophic mariculture waters. Like ciliates, the functional groups of phytoplankton may also be used as indicators of water quality,
although studies to date have tended to focus on freshwater,
as opposed to marine habitats (Reynolds et al. 2002).
Functional group
Habitat
Tolerances/sensitivities
A
B
C
D
E
F
G
H
I
J
K
L
M
Clean, cold water
Clean, warm water
Clean water
Clean, cold water
Clean, warm water
Slightly stressed, warm water
Slightly stressed, cold water
Moderately stressed, cold water
Moderately stressed, cold water
Moderately stressed, warm water
Moderately polluted, cold water
Heavily eutrophic, warm water
Severely polluted, warm water
Low temperature
High temperature, low salinity
High pH
Low temperature
High temperature
High temperature, slight pollutants
Low temperature, slight pollutants
Domestic and metal pollutants
Domestic and metal pollutants
Domestic and metal pollutants
Domestic and metal pollutants
Organic pollutants by mariculture eutrophication
Organic pollutants, nutrients and heavy metals
Environ Sci Pollut Res
It is noteworthy that the ciliates forming a single functional group often have different functions in the structuring
of communities or in response to environmental conditions.
For example, functional groups B and I, which comprised
mainly aloricate oligotrichids, were the primary component
in structuring the communities throughout almost the entire
period of study. By contrast, loricate (mainly tintinnid)
ciliate groups (e.g. group L) play a supporting role in functioning communities and sensitive to eutrophication and
pollution with high abundance, but only in summer and
autumn. Furthermore, in our previous studies, we confirmed
that non-loricate oligotrich ciliates are good surrogates for
planktonic ciliate communities in detecting their ecological
patterns at species level (Xu et al. 2011b; Jiang et al. 2012b).
The findings presented here are consistent with these.
Therefore, the non-loricate groups are potentially useful
bioindicators for marine bioassessment in large temporal
and spatial scales. In addition, in the case studies in specific
time periods and fixed environmental conditions, especially
in polluted and warm water areas, the functional groups with
loricate tintinnids could be a potential indicator.
Because their global distribution, ease of identification
and rapid response to environment change, the advantage of
using marine ciliated functional groups in bioassessment of
environmental quality is indubitability, and the application
potentiality and prediction feasibility of ciliate functional
groups to environmental conditions have been approved
by the present study. Further investigations on a range of
marine habitats and over extended time periods are needed
in order to verify this conclusion.
Conclusion
1. A total of 13 functional groups in marine ciliated protozoa were defined based on the specific characters in
terms of both spatio-temporal distribution and relationships to environmental conditions.
2. We provided basically and potentially functional information of functional groups to characterise and understand the
dynamics and distributions of marine ciliated protozoa.
3. Non-loricate ciliates and tintinnids represented different
roles in structuring and functioning of the communities.
4. The ciliated functional groups might be used as a potential bioindicator in assessment of water quality in
marine ecosystems.
Acknowledgments This work was supported by the “Natural
Science Foundation of China” (project nos. 41076089 and 41276139)
and the Darwin Initiative Programme (project no. 14–015) which is
funded by UK Department for Environment, Food and Rural Affairs.
We thank Mr. Jinpeng Yang, Mr. Wei Zhang, Dr. Xinpeng Fan, Dr. Jiamei
Jiang and Ms. Xumiao Chen, Laboratory of Protozoology, OUC, China,
for their help with sampling and sample processing.
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