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The first snapshot study on horizontal distribution and identification of five peritrich ciliates (Genus Vorticella Linnaeus and Zoothamnium Bory de St. Vincent) from the eastern Indian Ocean
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Sonia MUNIR1, 2, Jun SUN1, 2, *
Acta Oceanologica Sinica | 2018, 37(10) : 79 - 85
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Acta Oceanologica Sinica | 2018, 37(10): 79-85
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The first snapshot study on horizontal distribution and identification of five peritrich ciliates (Genus Vorticella Linnaeus and Zoothamnium Bory de St. Vincent) from the eastern Indian Ocean
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Sonia MUNIR1, 2, Jun SUN1, 2, *
Affiliations
  • 1 Tianjin Key Laboratory of Marine Resources and Chemistry, Tianjin University of Science and Technology, Tianjin 300457, China
  • 2 Research Centre for Indian Ocean Ecosystem, Tianjin University of Science and Technology, Tianjin 300457, China
Published: 2018-10-25 doi: 10.1007/s13131-018-1303-4
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Epipont peritrich ciliates are one of the most sessilie protists that attached to the substrate of zooplankton communities especially copepods and crustaceans. Peritrich ciliates can be solitary or colonial form found from the coastal zones and embayment around the world. Present research report is the first snapshot study of the peritrich ciliates and the horizontal distribution in open waters from surface to 200 m depth in the eastern Indian Ocean. Recently, five peritrich ciliates, e.g., Vorticella oceanica, Zoothamnium alternans, Z. alrasheidi, Z. pelagicum, and Z. marinum were collected from plankton net tow samples during the cruise from April 10 to May 13, 2014. The characteristics of the peritrich ciliate were determined according to the shape of the zooids, the ciliary structure and the stalks. The morphometric shape, sizes and characters also explained by examination under light/scanning electron microscopy. Vorticella oceanica and Z. pelagicum showed their association with host such as diatom (i.e, Chaetoceros coarctatus) and copepod (Oithona brevicornis) including some individuals around the dinoflagellate species (Ceraitum tripose). The distribution of these sessilid ciliates was dominated by the V. oceanica, Z. pelagicum and Z. marinum at the southeast zone while the large colonies of Z. alrasheidi observed at the Bay of Bengal. This distribution can be influenced by substrate availability like diatom (Ch. coarctatus) and copepods (O. brevicornis).

Vorticella oceanica  /  Zoothamnium alternans  /  Zoothamnium alrasheidi  /  Zoothamnium marinum  /  Zoothamnium pelagicum  /  eastern Indian Ocean
Sonia MUNIR, Jun SUN. The first snapshot study on horizontal distribution and identification of five peritrich ciliates (Genus Vorticella Linnaeus and Zoothamnium Bory de St. Vincent) from the eastern Indian Ocean[J]. Acta Oceanologica Sinica, 2018 , 37 (10) : 79 -85 . DOI: 10.1007/s13131-018-1303-4
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1 Introduction
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The class Oligohymenophora de Puytorac et al., 1974 and order Peritrichida has peritrich ciliates which characterized by its inverted bell shaped zooids, ciliary rows at the apical end and contractile stalks (Boltovskoy, 1999). Peritrich ciliates are both sesslie and planktonic protist of marine and freshwater environment which have mostly epibiotic attachment with crustaceans, e.g., scallops, blue crabs and zooplankton such as copepods (Fernandez-Leborans and Tato-Porto, 2000; Song et al., 2002; Gilbert and Schröder, 2003; Clamp and Williams, 2006; Ji et al., 2015; Sun et al., 2016), Amphipod (Fenchel, 1965), also attached to green microalgae like Chlorella sp. (Karakashian and Karakashian, 1965) and Ulva sp. (Ji and Song, 2004), diatoms Chaetoceros coarctatus and Licmophora (Nagasawa and Warren 1996; Gómez, 2017), and Cyanobacteria (Hausmann and Walz, 2007). Some of them also have been seen in association with microsporidia and trypanosomatid parasites (Fokin et al., 2014), Proteobacteria including Archaea (Schweikert et al., 2013) and other bacteria (Bauer-Nebelsick et al., 1996; Schuster and Bright, 2016). The epibiotic species of Vorticella, Zoothamnium and Epistylis have been found distributed in eutrophic biotopes such as coastal areas, e.g., Qingdao, China (Ji et al., 2009), Brazil (Regali-Seleghim and Godinho, 2004), Chesapeake Bay (Utz and Coats, 2005), Gulf of Mexico (Ma and Overstreet, 2006), Kayamkulam estuary of Kerala (Chitra and Kumar, 2015) and in shallow-water sunken wood in the North Adriatic Sea (Schuster and Bright, 2016). Although this epibiosis has wide distribution, it is still less prevalent than other microzooplanktons with the regard to similar congeners. However, it is difficult to understand its ecological prevalence in marine ecosystem. Sessilid ciliates have been reported worldwide but are unknown from the open sea, the eastern Indian Ocean. This baseline study on the distribution of peritrich ciliates and systematics is the key source for future research studies.
2 Materials and methods
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During springtime (April 10 to May 13, 2014), a total of 44 plankton net-hauled samples were collected from 200 m depth to the surface between the 10°N–5°S and 80°–95°E transect across the eastern Indian Ocean (Fig. 1). Samples were preserved by adding 2% formalin in 1 L Polycarbonate bottles. Only 3 mL of subsamples were used from each bottle and examined under the light microscope (Motic, AE2000) at 200× and 400× magnification. All light microscopic images captured using the Motic camera (2506, 5.6M) and scanning electron micrographs captured under the scanning electron microscopy (JEOL TM-5006). The sizes measured on the ocular micrometer scale under light microscope. The number of zooids separately counted by following the method of Liu et al. (2015) and converted into ind./m3.
3 Results and discussion
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Recently, a total of five species of peritrich ciliates (Vorticella oceanicum, Zoothamnium alternans, Z. alrasheidi, Z. marinum and Z. pelagicum) were collected from the open oceanic sampling sites at 200 m depth in the eastern Indian Ocean. Only V. oceanicum and Z. pelagicum are planktonic, free-floating Protista (Gómez, 2017). The Z. alternans, Z. alrasheidi, Z. marinum are mostly colonies former ciliates (Ji et al., 2009). During this study, V. oceanicum and Z. pelagicum although have specific host association with diatom Ch. coarctatus (Figs 2a, b), dinoflagellates species, Ceraitum tripose (Fig. 2c) and zooplankton such as copepods (i.e, Oithona brevicornis, Figs 2d, e).
Systematics and classification
Class Oligohymenophora de Puytorac et al., 1974
Subclass Peritrichia Stein, 1859
Order Sessilida Kahl, 1933
Family Vorticellidae Ehrenberg, 1838
Genus Vorticella Linneaus, 1767
Genus Zoothamnium Bory de St. Vincent, 1826
Family Vorticellidae
Vorticellidae family has been subjected to the taxonomic revision since 1838 by several authors (Ehrenberg, 1838; Song, 1991; Sommer, 1951; Stiller, 1971; Corliss, 1979; Kent, 1880–1882; Kahl, 1935; Lynn, 2008). Vorticellidae classified into two genera, Vorticella and Zoothamnium which have similar morphological characters, such as on the base of zigzag stalked with bell-shaped zooids and infraciliature structures. So far, more than 100 species of genus Vorticella and 70 species of genus Zoothamnium have been described (Song et al., 2009).
Genus Vorticella
The genus Vorticella is unique with its single cell having the contractile stalks. It can be differentiated to the other colony forming cells having elongated stalked ciliates Zoothamnium (Ehrenberg, 1838). Vorticella is widely distributed in coastal localities of China, Japan, Austria (Ji et al., 2005). Vorticella oceanica Zacharias, 1906 in association to Ch. coarctatus has been reported from Japan (Nagasawa and Warren, 1996), South Atlantic (Boltovskoy, 1999) and Brazil (Dias et al., 2006). This is the first record on the distribution of V. oceanica with attachment to Ch. coarctatus Lauder from the eastern Indian Ocean (Figs 2a, b).
Vorticella oceanica Zacharias, 1906
Description and distribution: Vorticella oceanica Zacharias, 1906 was observed with numerous single cells with cylindrical and somewhat elongated zooids that are attached to contractile stalks (Figs 3a, b). Single contractile vacuole (CV) is about 8 μm that are positioned to the ventral position with greenish granules on zooids pellicle. These zooids are attached to the diatom species Ch. coarctatus Lauder (Figs 2a, b). The zooids were measured up to 25–50 μm in size (Table 1). Zooids have middle ciliated rows along the oral cavity (Figs 3b–d). In the eastern Indian Ocean, these specimens were found high in cell numbers, e.g., 21–190 ind./m3 and distributed from the sampling sites at the southeast transect (Stas 1310, 1809, 1815, 1410 and 1511) and the Bay of Bengal (Stas 1609 and 1109) of this study area (Table 1) when temperature and salinity were recorded up to 22.25–24.11°C and 34.9 respectively.
Genus Zoothamnium
The genus Zoothamnium is colonized form of stalked type ciliates with cylindrical, vase shape and elongated zooids. These zooids connected to each other with smooth, long branch stalks and stalks disc. The species of Zoothamnium are complex in the external morphological traits, but the modern silver-impregnation techniques helped scientists to identify more than 70 species from this genus and many taxonomic reworks have been taken into consideration (Ji and Song, 2004; Ma and Overstreet, 2006; Ji et al., 2009). Some of them are reported from the South China Sea (Ji et al., 2009). Only one species, Zoothamnium pelagicum is a planktonic species which reported from the open sea, Meditternean Sea (Gómez, 2017). Four species, i.e., Z. alternans, Z. alrasheidi, Z. marinum and Z. pelagicum are reported for the first time from the eastern Indian Ocean (Figs 4 and 5).
Zoothamnium alternans Claparède et Lachmann, 1859
Zoothamnium alternans is cosmopolitan species and widely distributed in coastal areas of Qingdao, China (Ji et al., 2006), Gulf of Mexico (Ma and Overstreet, 2006). Zoothamnium alternans was described on the base of alternatively branched colony with large macro and microzooids that contain large teletrochs on the main stem and the J-shaped macronucleus (Song et al., 2009). Similar characteristics were observed for the species collected from the eastern Indian Ocean (Figs 4a–c).
Description and distribution: Each colony of Zoothamnium alternans is comprised of more than 30 to 50 zooids. The zooids were measured up to 30–87 μm in size. These zooids are attached with the smooth and long stalks (57–85 μm) which hinder with the large teletrochs (103 μm) located at the main trunk region (Figs 4a–c and Table 1). Zooids are mostly subglobular in shape, with ciliary rows, many greenish food-vacuoles, parallel silver lines, and contractile vacuoles (Figs 4a, b). This species often has long cilia (19 μm), contractile vacuole (8 μm) and peristomial lips (5 μm) (Fig. 4c). The specimens were collected from the sampling sites (Stas 1109, 1304 and 1807) that are located at the south-eastern part of the study area. The colonies were observed with maximum abundance (60 ind./m3) and have total numbers of zooids (560 m–3) when temperature and salinity were recorded up to 22.25–24.11°C and 34.9 respectively.
Zoothamnium alrasheidi Ji et al., 2009
Description and distribution: Zoothamnium alrasheidi were observed in the folliform, giant and leaf-shaped colonies. Each colony is comprised of more than 50 to100 zooids. The zooids were measured up to 37–40 μm in size. These zooids are attached with the smooth, long stalks (73 μm) without any teletrochs (Fig. 4d). Zooids are bottle shape with ciliary rows (Fig. 5d). The specimens were collected from the sampling site (Sta. 1609) located to the Bay of Bengal. More than three colonies were observed with a high abundance (58 ind./m3) and total number of zooids (1 948 m–3) (Table 1) during the low temperature and high salinity (23.35°C, 34.64).
Zoothamnium marinum Kahl, 1933
Zoothamanium marinum was the first described by Kahl in 1933. According to the original description, Z. marinum has the umbullate zooids with stalks devoid of any infraciliature and silverlines structures. This species can be differentiated with elongated zooids, single peristomial lips, and c-shaped macronucleus with single contractile myomene at the apical region of infundibular area of the oral cavity. Recently this species was reported from the littoral zones of Qingdao and South China Sea. This species was redescribed on the basis of transversely silverlines in the zooids between the peristomial lip and trochoband area (Ji et al., 2009).
Description and distribution: Zoothamanium marinum is elongated bell shaped and umberllate shaped colonies, consisting of no more than 24 zooids (Fig. 4e). The zooids were measured up to 30–55 μm in size. These colonies were collected from the sample sites (Stas 1304, 1307 and 1807), located at southeast part of the study area. The total colonies ranged into maximum abundance as 9–21 ind./m3 per colonies and total salinity observed from the ranges as 23.35–24.32°C and 34.64–35.00 respectively.
Zoothamnium pelagicum Du Plessis, 1891
Zoothamnium pelagicum was first described from the Mediterranean Sea by Du Plessis in 1891. Later this species also been reported from the same region (France and Spain) and South Atlantic Ocean (Gómez, 2017). Zoothamnium pelagicum has been classified as planktonic sessilid ciliates species, which are mostly associated to diatoms, Cyanobacteria and some bacteria (Laval-Peuto and Rassoulzadegan, 1988). This species has close resemblance with Z. alternans, Z. niveum and Z. plumula (Ji et al., 2015; Sun et al., 2016). This is the first report of Z. pelagicum (Figs 5a–f) in the eastern Indian Ocean.
Description and distribution: Zoothamnium pelagicum has inverted bell shaped zooids which consist more than 100 zooids in one colony (Figs 5a–h). Zooids with peristomial lips (Pl) and ciliary rows are shown in Fig. 5c. Each zooid was measured as 20–35 μm in size and attached to stalks disc. The stalks are smooth, elongated and 2 μm in width (Figs 5c–f and Table 1). This species were collected from the sampling sites located to southeast zone (Stas 1304, 1307, 1310 and 1807) and the Bay of Bengal (Sta. 1609) of the sampling area. Each colony was observed with high abundance 19–50 ind./m3 per colonies and total numbers of zooids are 827 ind./m3. Temperature and salinity was observed to be 24.25°C and 34.92 respectively.
Conclusion: The current study highlights the first report on the horizontal distribution and systematic studies of five peritich sessilid ciliates (Vorticella and Zoothamnium) from the eastern Indian Ocean. The Vorticella oceanica and Zoothamnium pelagicum are two major species which were observed with planktons, such as diatom (Chaetoceros coarcatus) and copepods (Oithona brevicornis). These planktonic ciliates are the source of nutrients recovered from the ecosystem. Most sessilid ciliates can increase high filtration rates and produce high biomass similar to other microzooplankton. This baseline study can play an important role in future research.
Acknowledgements
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The authors appreciate the support of the captain and crew of R/V Shiyan 1 and other participants, Ding Changling, Zhai Weidong, Wu Libin, Su Hongfei, Song Yongjun for trowlling and sampling in the eastern Indian Ocean.
Funding
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  • The NSFC Open Cruise for the Eastern Indian Ocean during March–May 2014; the National Natural Science Foundation of China under contract Nos 41876134, 41676112, 41276124 and 41406155; the University Innovation Team Training Program for Tianjin under contract No. TD12-5003; the Changjiang Scholar Program of Chinese Ministry of Education of China to Jun Sun.
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Article Info
doi: 10.1007/s13131-018-1303-4
  • Receive Date：2017-07-04
  • Online Date：2026-04-14
  • Published：2018-10-25
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History
  • Received：2017-07-04
  • Accepted：2018-04-10
Funding
The NSFC Open Cruise for the Eastern Indian Ocean during March–May 2014; the National Natural Science Foundation of China under contract Nos 41876134, 41676112, 41276124 and 41406155; the University Innovation Team Training Program for Tianjin under contract No. TD12-5003; the Changjiang Scholar Program of Chinese Ministry of Education of China to Jun Sun.
Affiliations
    1 Tianjin Key Laboratory of Marine Resources and Chemistry, Tianjin University of Science and Technology, Tianjin 300457, China
    2 Research Centre for Indian Ocean Ecosystem, Tianjin University of Science and Technology, Tianjin 300457, China

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表12种不同金属材料的力学参数
科
Family		 属数
Number of
genus		 种数
Number of
species		 占总种数比例
Percentage of
total species (%)		 属
Genus		 种数
Number of
species		 占总种数比例
Percentage of total
species (%)
鹅膏菌科Amanitaceae 2 11 5.26 鹅膏菌属 Amanita 10 4.78
小菇科 Mycenaceae 2 12 5.74 丝盖伞属 Inocybe 5 2.39
多孔菌科 Polyporaceae 8 14 6.70 蜡蘑属 Laccaria 5 2.39
红菇科 Russulaceae 3 23 11.00 小皮伞属 Marasmius 6 2.87
小菇属 Mycena 11 5.26
光柄菇属 Pluteus 5 2.39
红菇属 Russula 17 8.13
栓菌属 Trametes 5 2.39
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