PJZ_58_1_147-158

INTRODUCTION

Ciliates are unicellular, free-living aquatic characterized by cilia on their body surface (Hausmann and Hulsmann, 1996). Their size ranges from 20-200 µm are heterotrophic, although they also comprise mixotrophic forms (Stoecker et al., 1987). Mostly, they are holozoic and feed on algae, detritus, protists and bacteria. Some are carnivores and depend on small metazoans. Ciliates are an essential component of the microbial food web (Pierce and Turner, 1992). Mixotrophic ciliates are found simply in the aloricate sub-group (Stoecker et al., 1987) in the order Oligotrichida. According to the group division by Flynn et al. (2019) mixotrophic ciliates are part of non-constitutive mixotrophs, which are grazers that can keep their prey chloroplasts and can perform photosynthesis. Ciliates are microplankton and dominate marine microzooplankton communities in species abundance and number (De Vargas et al., 2015). They consume phytoplankton and serve as prey for metazoans therefore, they are an intermediate link in energy transfer in food webs (Fenchel, 2008). Worldwide studies on the diversity and distribution of the ciliates have been reported (Gomez, 2007; Yang et al., 2020).

Ciliates are extremely widespread across various habitats and environmental conditions (Wang et al., 2021). They are capable of turning into cryptobiotic forms when facing unfavourable conditions (Foissner et al., 2005), among which cyst formation is a common way to engage in resting and resistant stages and to support cell dispersion (Farmer, 1980). Red-coloured blooms of Mesodinium rubrum are reported in coastal waters occasionally in connection with upwelling. They are considered microzooplankton, their photosynthetic activity represents 70% of the contribution towards overall primary productivity (Crawford, 1989). Due to the blooms of Mesodinium rubrum, oxygen depletion occurs, which leads to fish kill in the coastal areas (Pau et al., 2017).

Ciliate communities are highly influenced by environmental factors such as salinity, nutrients, temperature, pH and biotic factors (predators) (Sun et al., 2017). Ciliates are found growing in some extreme environmental conditions, having sufficient vital energy to endure it (Lynn, 2008). Anaerobic ciliates are reported from anoxic environments, including marine, freshwater sediments, deep basins of estuaries and the anoxic hypolimnia of lakes (Finlay, 1982; Finlay et al., 1991; Fenchel et al., 1995; Xu et al., 2013). Ciliates are sporadically reported living in hot springs at temperatures greater than 40°C (Kahan, 1972). They are frequently found in several submarine hydrothermal vents. Twenty species of ciliates on the East Pacific Rise hydrothermal vents were reported by Small and Gross (1985). Ciliates were also reported in salt lakes having a pH value of 9.5 (Wilbert, 1995).

Hauer and Rogerson (2005) reported heterotrophic protozoan from hypersaline environments. According to their study, thirty species were identified from high salinity (>15%) waters. They elucidate that with an increase in salinities, species number of ciliates tends to decrease. In harsh Arctic and Antarctic environments, a number of research studies have been carried out to reveal the ecological role of planktonic marine ciliates (Roberts et al., 2004). However, spatial factors (dispersal) can also be considered in the case of ciliate community assemblage. The limitation in dispersal could lead to a reduction in community resemblance with distance (Pan et al., 2020). Studies have shown that the influence of environmental factors and spatial variables on ciliates mainly depends on the types of ecosystems and study scale (Zhang et al., 2018). The ciliate community structure in the middle pelagic zone is controlled by geographic distance and depth (Sun et al., 2019). In contrast, environments have a significant influence on ciliates than spatial factors in intertidal areas at the continental scale (Pan et al., 2020).

Planktonic marine microbes have an important role in biogeochemical cycles and form a link between bacteria and higher trophic levels (Azam et al., 1983; Caron et al., 1985). Ciliates have multifaceted ecological roles due to their morphological, trophic, genetic and metabolic diversity (Caron, 2016). These varied qualities shape the interspecific (parasitism, predation, etc.) interactions and species-environment and have a significant role in the assembling of marine ciliate communities (Fuhrman et al., 2015). The present research on the dynamics of ciliate species diversity, abundance and standing stocks would provide information on the functioning of marine ecosystems.

MATERIALS AND METHODS

For analysis of ciliates, seawater samples were collected from two sites, Gadani ship-breaking area and Sandspit. The samples of water were collected in four seasons from two sites for the period of one year (October 2016 – September 2017). Triplicate water samples were collected each month using a water sampler (Niskin 1.7L) from a 1-meter depth analyzed for water quality and abundance diversity were recorded employing standard methods. Ecological parameters temperature, salinity and pH were recorded on the sampling site. The water quality parameters of the sampling site were analyzed using respective instruments. Water temperature (mercury thermometer), salinity (Refractometer; Atago, Japan) and pH (pH meter). Dissolved oxygen (DO), nutrients (nitrate, nitrite, ammonia and phosphate) were estimated according to Strickland and Parsons (1972) method.

Abundance and diversity of the ciliates

For diversity and abundance of ciliates, triplicate water samples were collected and preserved in acid Lugol’s (1%) solution in 250 ml polycarbonated amber bottles. A sample volume of 50 ml was settled in a settling chamber (Hydrobios, Germany) for 24 h (Utermöhl, 1958). Ciliates were observed and counted under an inverted microscope (Olympus, IX-51 Japan). As a large number of species represented each genus, the counting was done for each species. The ciliates were identified on the basis of their characteristics for qualitative assessment.

Statistical analysis

Correlation coefficients (Pearson) between the ciliates density and the physiochemical parameters were determined. The data is analyzed using PRIMER 7.0. Changes in the ciliates community were examined using Shannon Weiner’s diversity (H’) and evenness (J).

RESULTS

The present investigation shows that the ciliate displayed a diverse species composition in Gadani and Sandspit in the Northern Arabian Sea. Seasonal abundance of ciliate was recorded in the present study. Seasons were categorized into Autumn Inter-Monsoon (October-November), Northeast Monsoon (December-February), Spring Inter-Monsoon (March-April) and Southwest Monsoon (May to September).

The ciliates diversity and abundance show variations in four seasons and vary from station to station. In Sandspit and Gadani, maximum abundance and diversity of ciliates was recorded in Southwest Monsoon (SWM) than in Spring Inter-Monsoon (SIM), Autumn Inter-Monsoon (AIM) and Northeast Monsoon (NEM) (Tables I-III). Ciliates species diversity in Gadani was more significant

Table I. Seasonal abundance of ciliates (cells/L) recorded from Gadani.

S. No.	Species	ST1	ST2	ST3
1	Acanthostomella minutissima	0	0	20
2	Acanthostomella norvegica	20	0	0
3	Amphorella brandti	20	0	0
4	Amphorella minor	40	0	20
5	Amphorellopsis acuta	40	0	0
6	Anigsteinia clarissima	140	180	40
7	Ascampbelliella retusa	0	20	20
8	Chaenea teres	160	20	80
9	Clevea melchersi	0	0	20
10	Codonella aspera	0	0	40
11	Codonella daday	20	0	40
12	Codonella galea	20	20	40
13	Codonella nationalis	20	40	100
14	Codonellopsis morchella	0	0	20
15	Codonellopsis schabi	0	0	20
16	Cyclotrichium gigas	0	0	40
17	Cyclotrichium sp	40	0	0
18	Cyrtophorid sp	140	0	0
19	Cyrtostrombidium longisomum	20	20	0
20	Cyttarocylis brandti	40	40	40
21	Cyttarocylis conica	20	20	20
22	Cyttarocylis magna	40	20	0
23	Daturella sp	40	0	0
24	Dictyocysta elegans	40	80	0
25	Didinium nasutum	20	0	20
26	Dysteria compressa	20	60	0
27	Epiplocyloides reticulata	0	0	40
28	Euplotes patella	0	0	20
29	Eutintinnus apertus	0	20	20
30	Eutintinnus attemtor	20	0	0
31	Eutintinnus attenuatus	0	0	20
32	Eutintinnus colligatus	20	20	20
33	Eutintinnus fraknoii	20	0	20
34	Eutintinnus lususundae	0	40	0
35	Eutintinnus rectus	20	20	20
36	Eutintinnus rugosus	0	0	40
37	Eutintinnus sp	0	40	0
38	Eutintinnus stramentus	20	20	60
39	Favella azorica	0	20	0
40	Favella campanula	20	0	20
	Table continues on next column................
S. No.	Species	ST1	ST2	ST3
41	Favella ehrenbergii	40	40	0
42	Geleia sp	140	60	20
43	Gruberia foissneri	20	0	0
44	Gruberia lanceolata	100	120	100
45	Helicostomella edentata	20	20	0
46	Helicostomella longa	20	0	40
47	Helicostomella subulata	0	20	0
48	Holosticha sp	0	100	0
49	Kentrophoros sp	0	40	0
50	Laackmanniella sp	20	0	0
51	Leprotintinnus simplex	220	160	20
52	Leprotintinnus nordqvistii	80	20	40
53	Leprotintinnus pellucidum	60	20	0
54	Litonotus fasciola	80	60	100
55	Mesodinium rubrum	0	20	0
56	Metacylis sp	0	20	20
57	Opercularia sp	0	0	20
58	Parallelostrombidium jankowski	40	0	20
59	Paramecium sp	40	0	40
60	Pelagacineta interrupta	0	0	20
61	Petalotricha ampulla	0	0	20
62	Petalotricha major	0	20	0
63	Poroecus curtus	0	0	20
64	Protorhabdonella simplex	40	80	0
65	Ptychocylis obtusa	0	0	20
66	Rhabdonella amor	0	0	20
67	Rhabdonella sp	0	20	0
68	Salpingacantha ampla	200	200	100
69	Salpingacantha nana	0	40	0
70	Salpingacantha pellucidum	40	0	0
71	Salpingacantha undata	20	0	20
72	Salpingacantha unguiculata	20	0	40
73	Salpingella acuminata	200	200	200
74	Salpingella ampla	20	0	60
75	Salpingella attenuata	100	60	80
76	Salpingella costata	0	0	20
77	Salpingella regulata	0	0	20
78	Salpingella rotundata	100	80	60
79	Spirostomum minus	20	0	80
80	Spirostomum sp	80	80	40
81	Steenstrupiella intumescens	0	20	40
82	Stentor polymorphus	0	0	20
83	Stentor sp	0	40	0
84	Strobilidium spiralis	40	100	0
85	Strombidinopsis sp	20	0	20
	Table continues on next page................
S. No.	Species	ST1	ST2	ST3
86	Strombidium conicoides	0	0	20
87	Strombidium conicum	120	40	40
88	Strombidium diversum	0	20	20
89	Strombidium guangdongense	0	0	20
90	Strombidium sp	60	60	0
91	Stylicauda platensis	0	20	20
92	Suctoria acineta	20	0	0
93	Tintinnopsis amphistoma	0	20	0
94	Tintinnopsis aperta	160	40	40
95	Tintinnopsis balechi	40	20	40
96	Tintinnopsis baltica	0	20	20
97	Tintinnopsis beroidea	220	200	120
98	Tintinnopsis campanula	0	20	0
99	Tintinnopsis corniger	40	20	60
100	Tintinnopsis cylindrical	120	80	160
101	Tintinnopsis dadayi	20	0	20
102	Tintinnopsis directa	20	0	0
103	Tintinnopsis esturiensis	0	40	0
104	Tintinnopsis everta	0	20	20
105	Tintinnopsis fimbriata	0	20	0
106	Tintinnopsis gracilis	80	300	160
107	Tintinnopsis lobiancoi	0	20	20
108	Tintinnopsis major	0	0	40
109	Tintinnopsis nana	40	40	60
110	Tintinnopsis orientalis	40	80	60
111	Tintinnopsis parva	100	20	80
112	Tintinnopsis parvula	80	0	20
113	Tintinnopsis radix	60	80	40
114	Tintinnopsis rapa	0	20	0
115	Tintinnopsis rotundata	20	20	40
116	Tintinnopsis stenosemella	0	40	0
117	Tintinnopsis tocantinensis	80	20	20
118	Tintinopsis compressa	40	0	0
119	Tokophrya sp	0	0	20
120	Tracheloraphis phoenicopterus	0	0	20
121	Undella globosa	20	20	20
122	Undella hemispherica	0	0	20
123	Undella hyalina	40	100	20
124	Undella pentagona	0	20	0
125	Undella subacuta	20	20	0
126	Undella turgida	40	0	20
127	Uroleptus sp	0	0	20
128	Zoothamnium elegans	20	0	20
	Genera: 56; Species: 128	4300	3780	3480

Rare = 1-150 * Common = 151-250** Dominant = 251-350< ***

Table II. Seasonal abundance of ciliates (cells/L) recorded from Sandspit.

S. No.	Species	ST1	ST2
1	Amphorella brandti	0	20
2	Anigstenia clarissima	220	200
3	Chaenea teres	140	40
4	Codonella galea	60	0
5	Codonella nationalis	40	0
6	Codonellopsis gaussi	20	20
7	Codonellopsis morchella	20	0
8	Cyttarocylis magna	40	40
9	Dadayiella sp	0	60
10	Epiplocylis blanda	20	20
11	Epiplocylis undella	20	0
12	Eutintinnus apertus	40	200
13	Eutintinnus elongatus	20	120
14	Eutintinnus fraknoii	0	20
15	Eutintinnus rectus	40	0
16	Eutintinnus stramentus	60	20
17	Favella azorica	20	20
18	Favella ehrenbergii	40	0
19	Favella markusouzkyi	40	0
20	Gruberia lanceolata	120	100
21	Helicostomella subulata	0	20
22	Laboea strobila	20	20
23	Lacrymaria olor	20	40
24	Leprotintinnus nordqvistii	120	80
25	Leprotintinnus pellucidum	20	20
26	Leprotintinnus simplex	160	320
27	Litonotus fasciola	100	60
28	Mesodinium rubrum	80	40
29	Metacylis jorgensenii	0	20
30	Paramecium sp	40	0
31	Parundella aculeata	20	20
32	Petalotricha ampulla	20	0
33	Philasterides armatali	20	0
34	Protorhabdonella striatura	0	20
35	Ptychocylis obtusa	0	20
36	Ptychocylis sp	60	0
37	Salpingacantha ampla	360	120
38	Salpingacantha perca	0	40
39	Salpingacantha undata	0	20
40	Salpingacantha unguiculata	20	0
41	Salpingella acuminata	260	260
42	Salpingella attenuata	140	40
	Table continues on next page................
S. No.	Species	ST1	ST2
43	Salpingella decurtata	80	40
44	Salpingella rotundata	40	20
45	Spirostomum ambiguum	80	40
46	Spirostomum minus	180	220
47	Steenstrupiella gracilis	160	80
48	Steenstrupiella inteumescens	20	0
49	Steenstrupiella steenstrupii	40	0
50	Stenosemella sp	20	60
51	Strobilidium spiralis	40	40
52	Strombidium conicum	220	260
53	Strombidium elongatum	120	40
54	Strombidium oculatum	60	40
55	Thuricola folliculata	20	20
56	Tintinnopsis balechi	20	0
57	Tintinnopsis beroidea	160	0
58	Tintinnopsis campanula	180	120
59	Tintinnopsis choroestrichids	20	0
60	Tintinnopsis corniger	20	0
61	Tintinnopsis cylindrical	40	40
62	Tintinnopsis dadayi	180	100
63	Tintinnopsis everta	20	0
64	Tintinnopsis fistularis	20	20
65	Tintinnopsis gracilis	100	40
66	Tintinnopsis hemispiralis	0	20
67	Tintinnopsis karajacensis	20	0
68	Tintinnopsis kofoidi	20	0
69	Tintinnopsis lobiancoi	40	60
70	Tintinnopsis nana	20	0
71	Tintinnopsis parva	120	200
72	Tintinnopsis parvula	20	40
73	Tintinnopsis radix	120	140
74	Tintinnopsis redixand	40	0
75	Tintinnopsis rotundata	80	200
76	Tintinnopsis tocantinensis	100	60
77	Tintinnopsis ventricosoides	40	20
78	Trachelophyllum apiculatum	20	0
79	Trochilia sigmoides	20	60
80	Undella hyalina	120	100
81	Undella subacuta	20	0
82	Undella turgida	20	20
83	Xystonella treforti	0	20
	Genera: 37, Species: 83	5080	4160

Rare= 1-150 * Common= 151-250** Dominant= 251-350< ***

Table III. Seasonal abundance of ciliates (cells/L) recorded from Gadani and Sandspit.

Localities/ No. of seasons	Total No. of individuals (Cells/L)	Margalef richness index	Pielou's evennes index	Shanon diversity index
Gadani
AIM	88	0.44669	0.99988	1.0985
NEM	161	0.39359	0.97338	1.0694
SIM	80	0.45641	0.93723	1.0297
SWM	250	0.36222	0.98401	1.081
Sandspit
AIM	88	0.22335	0.99664	0.69082
NEM	118	0.20961	0.93925	0.65104
SIM	80	0.2282	0.97095	0.67301
SWM	176	0.19341	0.99767	0.69153

For details of abbreviations, see Figure 2.

as compared to Sandspit. The total number of 128 species of ciliates classified into 56 genera from Gadani and 83 species of ciliates classified into 37 genera from Sandspit were recorded. Twenty-six species of Tintinnopsis were observed in Gadani, whereas twenty-two species of Tintinnopsis were observed in Sandspit (Tables I, II). The seasonal abundance of ciliates genera (cells/L) from Gadani and Sandspit are depicted in Figures 2 and 3. The high values of the Shannon diversity index were 1.0985 in Gadani and 0.69153 in Sandspit. Richness was high in SIM on both sites. Evenness was high in AIM in Gadani while SWM in Sandspit (Table III). The physicochemical parameters recorded from Gadani and Sandspit are shown in Figure 1.

Pearson correlation coefficient (Table IV) was used to detect the association among ciliate communities with hydrographical parameters and nutrients. Ciliates abundance was correlated with salinity, dissolved oxygen and chlorophyll a while negative correlation was detected with temperature, pH, nitrite, nitrate, phosphate and ammonia in station 1 at Gadani. Whereas in station 2, Ciliates abundance was negatively correlated with hydrographical parameters and nutrients. In station 3, ciliates abundance was correlated with salinity, pH, dissolved oxygen, nitrite, nitrate, ammonia and chlorophyll a while negative correlation was detected with temperature and phosphate. In Sandspit (Table V) in station 1, ciliates abundance was negatively correlated with hydrographical parameters and nutrients. While in station 2, ciliates abundance was positively correlated with temperature, salinity, pH,

Table IV. Pearson correlation coefficient between ciliates communities with environmental variables in Gadani.

ST 1	Abundance	Temp	Salinity	pH	Oxygen	Nitrate	Nitrite	Phosphate	Ammonia
Temp	-0.267
Salinity	0.012**	-0.169
pH	-0.079	0.101 ns	0.791 ns
Oxygen	0.123ns	0.061	0.477 ns	0.843 ns
Nitrate	-0.077	0.077	0.825 ns	0.988 ns	0.810 ns
Nitrite	-0.038	0.083	0.849ns	0.951 ns	0.763ns	0.985ns
Phosphate	-0.276	0.378 ns	0.304 ns	0.435ns	0.308ns	0.475 ns	0.509 ns
Ammonia	-0.068	0.272 ns	0.708 ns	0.876ns	0.689ns	0.875 ns	0.854 ns	0.299ns
Chlorophyll	0.482 ns	0.405 ns	-0.205	0.021*	0.358 ns	0.026*	0.07	0.149ns	0.157 ns
ST 2
Temp	-0.282
Salinity	-0.512	-0.169
pH	-0.456	0.101ns	0.791ns
Oxygen	-0.378	0.061	0.477 ns	0.843ns
Nitrate	-0.406	0.077	0.825 ns	0.988 ns	0.810ns
Nitrite	-0.37	0.083	0.849 ns	0.951 ns	0.763ns	0.985ns
Phosphate	-0.138	0.378 ns	0.304 ns	0.435ns	0.308 ns	0.475ns	0.509ns
Ammonia	-0.496	0.272ns	0.708 ns	0.876ns	0.689ns	0.875 ns	0.854ns	0.299ns
Chlorophyll	-0.12	0.405ns	0.205 ns	0.021*	0.358ns	0.026*	0.07	0.149ns	0.157 ns
ST 3
Temp	-0.307
Salinity	0.302 ns	-0.169
pH	0.165 ns	0.101 ns	0.791ns
Oxygen	0.130 ns	0.061	0.477ns	0.843 ns
Nitrate	0.138ns	0.077	0.825 ns	0.988 ns	0.810 ns
Nitrite	0.128ns	0.083	0.849 ns	0.951 ns	0.763ns	0.985 ns
Phosphate	-0.164	0.378 ns	0.304ns	0.435ns	0.308ns	0.475 ns	0.509 ns
Ammonia	0.209 ns	0.272 ns	0.708ns	0.876 ns	0.689 ns	0.875 ns	0.854ns	0.299 ns
Chlorophyll	0.268 ns	0.405 ns	0.205 ns	0.021*	0.358ns	0.026*	0.07	0.149 ns	0.157 ns

*Represents significant at p < 0.05, **represents significant at p < 0.01 and ns represents non-significant.

dissolved oxygen, nitrate, nitrite and ammonia, while a negative correlation was detected with phosphate and chlorophyll a.

DISCUSSION

In Sandspit and Gadani, maximum abundance and diversity of ciliates was recorded in the SWM than in the SIM, AIM and NEM. In the Southwest Monsoon, the more vigorous upwelling in the Northern Indian Ocean leads to high primary productivity (Goes, 2005). High primary productivity may be linked to temperature that increases during the SWM (May to September). Previous studies reported that the ciliate diversity is greatly influenced by temperature and salinity (Xu et al., 2018). Temperature affects the ciliates primarily by controlling their growth (Montagnes and Lessard, 1999). The salinity of the water increases with the rise in temperature. The ciliates can tolerate extreme changes in salinity, and some ciliates can withstand direct transfer from marine coastal areas to fresh waters (Smurov et al., 2013). In high temperatures in the SWM, the organisms demand for oxygen increases, resulting in low dissolved oxygen retaining capacity of water (Hussain et al., 2013). Ciliates are sensitive to changes in the concentration of oxygen in water (Fenchel, 2012). The diversity of the ciliates in marine waters also depends on the constancy of the oxygen gradients.

Table V. Pearson correlation coefficient between ciliates communities with environmental variables in Sandspit.

ST 1	Abundance	Temp	Salinity	PH	Oxygen	Nitrate	Nitrite	Phosphate	Am-monia
Temp	-0.607
Salinity	-0.318	0.158
pH	-0.107	-0.08	-0.107
Oxygen	-0.007	-0.104	-0.109	0.096
Nitrate	-0.214	-0.019	0.421ns	-0.383	0.134 ns
Nitrite	-0.344	-0.035	-0.053	0.379 ns	0.089	0.478ns
Phosphate	-0.103	-0.167	-0.297	0.448ns	-0.171	-0.096	0.288 ns
Ammonia	-0.117	0.243 ns	0.435 ns	-0.126	0.006**	0.539 ns	0.057*	-0.449
Chlorophyll	-0.295	0.470ns	0.118ns	-0.61	0.237 ns	0.441ns	-0.076	-0.335	0.301 ns
ST 2
Temp	0.233 ns
Salinity	0.102 ns	0.158 ns
pH	0.217 ns	-0.08	-0.107
Oxygen	0.127ns	-0.104	-0.109	0.096
Nitrate	0.190 ns	-0.019	0.421ns	0.383	0.134 ns
Nitrite	0.422 ns	-0.035	-0.053	0.379 ns	0.089	0.478
Phosphate	-0.35	-0.167	-0.297	0.448 ns	-0.171	-0.096	0.288ns
Ammonia	0.387 ns	0.243ns	0.435ns	-0.126	0.006**	0.539 ns	0.05*	-0.449
Chlorophyll	-0.134	0.470 ns	0.118 ns	-0.61	0.237 ns	0.441ns	-0.07	-0.335	0.301ns

*Represents significant at p < 0.05, **represents significant at p < 0.01 and ns represents non-significant.

In the SWM, the peak abundance of ciliates was observed due to high chlorophyll a content in Gadani and Sandspit. Our results are in agreement with Soriede et al. (2010), who stated that the abundance of microzooplankton may be linked to the high chlorophyll a in the area. Chlorophyll a distribution depends on physico-chemical concentrations, for example, nutrients and temperature (Lakkis et al., 2003). Nutrients and climate changes (wind patterns and rainfall) in coastal areas also influence ciliate diversity and communities (Lopez-Abbate et al., 2019; Zhu et al., 2020). The diversity of species in Gadani was more remarkable as compared to Sandspit. The total number of 128 species of ciliates classified into 56 genera from Gadani and 83 species of ciliates classified into 37 genera from Sandspit were recorded. The abundance, diversity and survival of organisms initiate in favourable environments, nutrient-rich and less predation sites (Cocheret de la Moriniere et al., 2004). Pollutants in marine environments are known to reduce species diversity and increase the population of tolerant species. In Sandspit, the most dominant ciliate species were Leprotintinnus simplex, Salpingacantha ampla, Salpingella acuminata, Spirostomum minus and Strombidium conicum. However, in Gadani, the most dominant species of ciliates were Salpingella acuminata, Tintinnopsis beroidea and Tintinnopsis gracilis.

In Sandspit and Gadani, we observed that the diversity of ciliates increases in near-shore waters as compared to shore and offshore waters. This is in agreement with previous studies that the diversity of ciliates reduced with an increase in distance from shore (Tamura et al., 2011). Ocean currents impact the waters from oceanic and neritic zones and are homogenous with the same hydrological characteristics, resulting in remarkable similarity of organisms. The importance of ciliates in energy transfer in marine food webs is well-known in ecological function (Fenchel, 1988). The abundance of ciliates in marine waters is controlled by zooplankton, especially filter-feeding copepods (Atikinson, 1996). Ciliates are primary grazers on bacterioplankton and nanoplankton (Premke and Arndt, 2000). Moreover, planktonic algae, bacteria and mesozooplankton have substantial effects on the diversity and abundance of ciliate communities (Yang et al., 2020). Many scientists have confirmed that ciliate abundance can be influenced by environmental factors comprising nutrients, pH, salinity, temperature and biotic interactions, for example, predators (Gimmler et al., 2016; Sun et al., 2017). However, spatial factors have also been considered in the study of ciliate community assemblage. The limitation in dispersal would lead to a decrease in community similarity with distance (Pan et al., 2020). The effect of environmental and spatial variables on ciliates depends on the study scale and kind of environment (Zhang et al., 2018). The ciliate community structure in the mesopelagic zone is controlled by geographic distance and ocean depth (Sun et al., 2019).

Planktonic ciliates are frequently dominated by aloricate ciliates (Leakey et al., 1996). However, many studies are focused on tintinnids (Rakshit et al., 2014) owing to difficulties in the identification which mislead the contribution of these aloricate ciliates. Previous studies reported aloricate ciliates numerically dominant than tintinnids in the central and western Arabian Sea (Leakey et al., 1996) in the Northern Arabian Sea (Siddiqui et al., 2000; Burhan et al., 2018). However, in our studies, tintinnids were more dominant than aloricate in both Gadani and Sandspit. From Sandspit, eighteen species of aloricate ciliates are recorded, while loricate is sixty-five species in number. In Gadani, thirty-eight species of aloricate ciliates are recorded, while loricate is ninety species in number.

Tintinnids are unicellular loricate ciliates (Montagnes, 2013) that inhabit freshwaters and marine environments (McManus and Santferrara, 2013). They play an essential role in the food chain that feeds on bacteria and phytoplankton, they, in turn, serve as food for larger marine organisms, for example, copepods and fish larvae (Stoecker, 2013). Tintinnids are used as bioindicators to assess environmental stress and anthropogenic impacts on marine ecosystems (Jiang et al., 2011; Xu et al., 2011) and to monitor aquatic water quality (Wu et al., 2016). Due to their delicate pellicles and short life cycles, they respond quickly to environmental changes (Ismail and Dorgham, 2003). Twenty-six species of Tintinnopsis are present in Gadani, whereas twenty-two species of Tintinnopsis are present in Sandspit. Many ciliates are more resistant to extreme environmental conditions than macrofauna (Xu et al., 2011). The dominant species of Tintinnopsis in Gadani and Sandspit coastal waters agrees with that reported by Jiang et al. (2011) and Feng et al. (2015). Tintinnopsis abundance may be related to their adaptive nature or sustaining in eurythermal and euryhaline aquatic environments. The ciliates are vulnerable to environmental variants, and the pollution arising from industrial units alongside the coastal areas is hazardous for fish. There is an essential requirement for monitoring of ciliates with respect to abundance, diversity, distribution and harmful algal bloom-forming species as it affects the fishery industry and marine environment.

Declarations

Acknowledgement

The authors would like to thank the Higher Education Commission (HEC), Islamabad, Pakistan, for providing funds to carry out the present research. The facilities provided by the Centre of Excellence in Marine Biology are well appreciated.

Conflict of interest

The authors declare that there is no conflict of interest regarding the publication of this article.

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