A new tintinnid ciliate (Ciliophora: Spirotrichea) from Yangtze River

Zoological Systematics, 39(3): 372–379 (July 2014), DOI: 10.11865/zs20140303
ORIGINAL ARTICLE
A new tintinnid ciliate (Ciliophora: Spirotrichea) from Yangtze
River Estuary, with notes on its habitat
Wu-Chang Zhang1*, Mei-Ping Feng1, 2, Ying Yu1, 2, Xu-Miao Chen1, Tian Xiao1
1
Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, China
University of Chinese Academy of Sciences, Beijing 100049, China
2
*Corresponding author, E-mail: [email protected]
Abstract A new tintinnid ciliate, Tintinnopis estuariensis sp. nov. was found in the estuary
of Yangtze River, China. It was most abundant in September. Its arenaceous lorica is
cylindro-conical in shape, (120–180) μm × (50–75) μm in size, agglutinated with mineral
particles, and open at both ends. Two characters distinguish it from others: the unique lateral
flattened posterior portion with a vertical aboral opening and wider oral diameter. It occurred
in water with surface temperature of 14–27°C and surface salinity of 3.9‰–29.8‰.
Key words Taxonomy, Tintinnida, lorica, new species.
1
Introduction
Tintinnids are important parts of microplankton communities, and are considered as primary mediators of energy
transfer from pico- and nanoplankton to higher trophic levels in the microbial food webs (Dolan, 2013). They are
characterized by species-specific loricae, which have various shapes ranging from tubular to vase- or bowl-shaped (Dolan,
2013). The lorica is always open at the oral end, while the aboral end, which is opposite the oral end, is closed or open.
The characteristics of the lorica provide critical distinction for tintinnid taxonomic identification (Lynn, 2008; Dolan,
2013). In the report, a new tintinnid ciliate, Tintinnopsis estuariensis sp. nov. is found in the estuary of Yangtze River,
China.
To date, 930 contemporary species of tintinnids are reported under 67 genera of 15 families in marine and freshwaters
all over the world (Zhang et al., 2012b). The genus Tintinnopsis is the largest genus of the family Codonellidae, even
among the order Tintinnida, due to their highly variable loricae (Zhang et al., 2012b). The genus is characterized by totally
agglutinated lorica (whole lorica is covered with accreting particles). However, it is still very hard to identify because the
particles covering the lorica obscure the structure of the lorica (Kofoid & Campbell, 1929; Alder, 1999). So far, for the
studies on the infraciliature, only 12 species among the 140 species in the genus Tintinnopsis have been reported (Jiang et
al., 2012; Zhang et al., 2012b).
2
Materials and methods
Specimens were collected from 40 stations in the estuary of Yangtze River (30.5–32.5°N, 121.0–123.5°E, Fig. 1)
during four periods in 2005: February 27–March 11, May 29–June 5, September 7–15 and November 17–26. The depth of
water at the stations ranged from 3 m to 64 m. Samples were collected by a vertical towing plankton net (open area 0.1 m2,
mesh size 76 μm) from the bottom to the surface and then the samples were saved in 2% formalin solution. Water
urn:lsid:
Received 18 April 2013, accepted 18 November 2013.
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New tintinnid species from Yangtze River
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temperature and salinity were measured and recorded using CTD system. Type specimens were deposited in the Key
Laboratory of Marine Ecology and Environmental Sciences, Institute of Oceanology, Chinese Academy of Sciences.
The measure is done by an inverted microscope (Olympus IX71) with the help of photomicrographic system.
Fifty-two specimens were randomly selected to measure the dimensions of the loricae. Each specimen was gently turned to
obtain tridimensional measurements. The following dimensions of the lorica were measured: total length (L), oral diameter
(OD), length of cylinder portion (CL), length of tapered portion (TL), height of the flare (HF), aboral opening diameter
along the major axis (AODMA), and aboral opening diameter along the minor axis (AODMI). Lorica architecture was
photoed using a KYKY-2800 scanning electron microscope (SEM). The loricae were prepared according to the method of
Wasik and Mikolajczyk (1991). A thorough search of the literature (Kofoid & Campbell, 1929, 1939; Zhang et al., 2012b)
was conducted.
Fig. 1. Sampling stations in the estuary of Yangtze River in 2005.
Fig. 2. Tintinnopsis estuariensis sp. nov., six different individuals with same scale. Scale bar=50 μm.
© Zoological Systematics, 39 (2): 372–379
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Zhang et al.
To estimate the abundance of the new species, a 2 ml subsample of each fixed sample was pipetted into a
sedimentation chamber and the abundance of T. estuariensis was determined using an Olympus IX71 microscope at ×100
or ×200 magnification.
3
Results
Phylum Ciliophora Doflein, 1901
Class Spirotrichea Bütschli, 1889
Subclass Choreotrichia Small & Lynn, 1985
Order Tintinnida Kofoid & Campbell, 1929
Family Codonellidae Kent, 1881
The new species is classified as genus Tintinnopsis because its lorica is totally agglutinated with mineral particles, the
collar is absent, it is non-spiralled or irregularly spiralled, and has a vertical aboral opening, which is consistent with the
taxonomic features of the genus Tintinnopsis as described by Alder (1999).
Fig. 3. SEM images of major axis in Tintinnopsis estuariensis sp. nov. Scale bars: A=100 μm; B – C=10 μm.
© Zoological Systematics, 39 (2): 372–379
New tintinnid species from Yangtze River
Tintinnopsis estuariensis sp. nov.
375
(Figs 2–3, Tables 1–2)
Diagnosis. The species is distinguished from other species by: cylindro-conical shaped lorica with a lateral flattened
posterior portion (Fig. 2).
Table 1. Lorica measurements of Tintinnopsis estuariensis sp. nov. (n=52).
Characteristics (μm)
Min
Max
Mean
SD
CV
L
124
176
157
9.1
5.8
OD
55
72
64
3.0
4.7
AODMA
13
37
24
5.1
21.1
AODMI
7
23
14
2.9
20.8
HF
6
26
15
3.7
24.2
CL
71
113
90
9.0
10.1
TL
45
90
67
11.4
17.0
Note. Min, minimum; Mean, arithmetic mean; Max, maximum; SD, standard deviation; CV, coefficient of variation in %.
Fig. 4. Distribution of surface temperature (T, °C), salinity (S, ‰) and abundance (Abun, ind./ m3) in May, September and
November of 2005.
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Zhang et al.
Table 2. Ratio among the lorica measurements of Tintinnopsis estuariensis sp. nov. (n=52).
Ratio characteristics
Min
Max
Mean
SD
CV
HF/L
0.04
0.15
0.10
0.02
20.0
CL/L
0.44
0.71
0.57
0.06
10.5
TL/L
0.29
0.56
0.43
0.06
14.0
TL/OD
2.09
2.81
2.44
0.15
6.2
AODMA/AODMI
1.06
3.60
1.78
0.50
28.1
OD/AODMA
1.60
4.85
2.79
0.62
22.2
Note. Min, minimum; Mean, arithmetic mean; Max, maximum; SD, standard deviation; CV, coefficient of variation in %.
Description. Lorica 124–176 μm long and 55–72 μm wide orally (measured in this paper), totally covered with flakes
of mineral particles (Figs 2–3); cylindro-conical shaped with a lateral flattened posterior portion and open at both ends (Fig.
2); the upper 44%–71% of the lorica cylindrical and the lower 29%–56% flattened; flare 6–26 μm long at the oral end and
no collar; aboral opening diameter along the major axis 13–37 μm, aboral opening diameter along the minor axis 7–23 μm
(Table 1); oral rim round and the aboral end ragged (Fig. 3).
Holotype, China, Yangtze River Estury (31.5°N, 122.2°E), September 2005, Wu-Chang Zhang, deposited in the Key
Laboratory of Marine Ecology and Environmental Sciences, Institute of Oceanology, Chinese Academy of Sciences.
Paratypes 20 individuals, same data as holotype.
Habitat. The species is found in the estuary of Yangtze River, China. Temporally, Tintinnopsis estuariensis was most
abundant in September, 32 410 ind./m3 in max. The species also occurred in May and November with maximum abundance
of 17 070 ind./m3 and 1 357 ind./m3 respectively. No individuals were found in February. Tintinnopsis estuariensis occurred
in waters with a surface temperature of 14–27°C (Fig. 5).
By analyzing surface salinity of 40 stations (Figs 4–5), Tintinnopsis estuariensis can be alive in water with a surface
salinity of 3.9‰–29.8‰, especially water with surface salinity below 21‰, which has abundance larger than 800 ind./m3.
Etymology. The species name estuariensis reflects its the typical location.
Comparison. The new species is similar with several species of Tintinnopsis on the tube shape and lorica size, a
comparison is provided (Table 3, Fig. 6). The new species differed from its congeners due to the lateral flattened posterior
portion, the vertical aboral opening and the wider oral opening.
Fig. 5. Surface water temperature (°C) and salinity (S, ‰) in the sampling sites during four cruises in the estuary of Yangtze River in
2005. Different sizes of circles indicates different abundances (ind./ m3) of Tintinnopsis estuariensis sp. nov. in the sampling site,
and the solid dots means no individual were found in the according site.
© Zoological Systematics, 39 (2): 372–379
Table 2. Comparison of Tintinnopsis estuariensis sp. nov. and its allied species.
Species
Posterior portion
Aboral opening
L (μm)
OD (μm)
Occurrence in record
Reference
T. estuariensis
T. akkeshiensis
Lateral flattened
Conical
124–176
50–112
55–72
24–34
Yangtze River estuary (14–27°C)
Akkeshi Bay (8–15.3°C)
In present
Hada, 1937
T. cylindrica
Gradually tapering
into a bluntly pointed
and sometimes slight
curved aboral end
Vertical opening
Situated laterally and
rarely obliquely
Opening at the end
238–355
144–300
120–223
-
40–60
34–45
35–42
-
Bay of Naples
Bay of Amoy in the East China Sea
Mediterranean, Baltic, western Pacific
Coastal waters of the Southwest Netherlands
Nervion River estuary
North Sea
T. kofoidi
Conical aboral horn
Obliquely opening at the
tip
T. sufflata
Conical
70
35–40
21–24
35–42
19–21
Coastal waters in the South China Sea
Sea of Okhotsk (10.0–16.4 °C)
Mutsu Bay
Akkeshi Bay (8.7–18.2 °C)
Atlantic
New York Bight
South Atlantic
Jiaozhou Bay in the Yellow Sea
Akkeshi Bay (7.0–16.3°C)
T. radix
Conical
Laterally or obliquely
irregular aboral opening
Opening at the tip
335
156–188
70–100
150–225
50–65
Kofoid & Campbell, 1929
Wang & Nie, 1932
Marshall, 1934
Bakker & Phaff, 1976
Urrutxurtu, 2004
Agatha & Riedel-Lorje,
2006
Zhang et al., 2012a
Hada, 1932a
Hada, 1932b
Hada, 1937
Balech, 1948
Gold & Morales, 1975
Alder, 1999
Zhao et al., 2007
Hada, 1937
260–416
353–502
40–45
46–61
330–492
296
225–496
107–525
225–343
263–352
250–262
269–410
400
-
40–46
45
33–56
38–40
40–49
39
43–46
50
-
Off Bagamojo, Zanzibar
Mutsu Bay
Coasts of Mediterranean and Atlantic, Indian and
Pacific Oceans
Bay of Amoy in the East China Sea
Akkeshi Bay (17.3 °C)
Western tropical Pacific
Jiaozhou Bay in the Yellow Sea
Mediterranean
Atlantic coast of Uruguay and southern Brasil
Strait of Hormoz and the United Arab Emirates waters
South Atlantic
Southwestern Atlantic
Coastal waters of Qingdao in the Yellow Sea
Northern South China Sea
Note. L, total length; OD, oral diameter.
Kofoid & Campbell, 1929
Hada, 1932b
Marshall, 1934
Nie, 1934
Hada, 1937
Hada, 1938
Yin, 1952
Balech, 1959
Souto, 1970
Sharaf, 1995
Alder, 1999
Fernandes, 2004
Xu & Song, 2005
Feng et al., 2010
378
Zhang et al.
Remarks. Although most taxonomic studies on tintinnids have been based on the lorica, there are reports of large
variations in the shape of loricae in the same species in the genera Favella, Parafavella and Ptychocylis (Laval-Peuto,
1981; Davis, 1978, 1981). Therefore, modern taxonomy of tintinnid requires cytological characteristics such as
infraciliature. However, there are no reports on a large variation in lorica shape in the genus Tintinnopsis. These data
should be added in future research.
Fig. 6 Tintinnopsis estuariensis sp. nov. and its allied species. A. T. estuariensis; B. T. akkeshiensis; C. T. sufflata; D. T. kofoidi; E. T.
radix; F. T. cylindrical. B and C after Hada (1937); D after Hada (1932a, b, 1937), Balech (1948), Alder (1999) and Zhang et al.
(2012b); E after Kofoid and Campbell (1929), Xu and Song (2005); F after Kofoid and Campbell (1929) and Zhang et al. (2012a).
Scale bar=50 μm.
Funding This study was supported by the National Basic Research Program of China (973 Program) (2011CB409804)
and the National Natural Science Foundation of China (U1406403).
References
Agatha, S. and Riedel-Lorje, J. C. 2006. Redescription of Tintinnopsis cylindrica Daday, 1887 (Ciliophora: Spirotricha) and unification
of tintinnid terminology. Acta Protozoologica, 45(2): 137–151.
Alder, V. 1999. Tintinnoinea. In: Boltovskoy, D. (ed.), South Atlantic Zooplankton. Backhuys Publishers, Leiden. pp. 321–384.
Bakker, C. and Phaff, W. J. 1976. Tintinnida from coastal waters of southwest Netherlands 1. Genus Tintinnopsis Stein. Hydrobiologia,
50: 101–111.
Balech, E. 1948. Tintinnoinea de Atlantida (R. O. del Uruguay) (Protozoa Ciliata Oligotr.). Comun. Mus. Argent. Cienc nat. Bernardino
Rivadavia, Ser. Cienc. Zool., 7: 1–23.
Balech, E. 1959. Tintinnoinea del Mediterraneo. Trab. Inst. Espan. Oceanogr., 28: 1–88.
© Zoological Systematics, 39 (2): 372–379
New tintinnid species from Yangtze River
379
Davis, C. C. 1978. Variations of lorica in the genus Parafavella (Protozoa: Tintinnia) in northern Norway waters. Canadian Journal of
Zoology, 56: 1822–1827.
Davis, C. C. 1981. Variations of lorica shape in the genus Ptychocylis (Protozoa: Tintinnia) in relation to species identification. Journal
of Plankton Research, 3(3): 433–443.
Dolan, J. R. 2013. An introduction to tintinnids. In: Dolan J. R., Agatha S., Coats D. W., Montagnes D. J. S. and Stocker D. K. (eds.),
Biology and Ecology of Tintinnid Ciliates: Models for Marine Plankton. Wiley-Blackwell, Oxford. pp. 1–16.
Feng, M-P, Zhang, W-C, Zhang, C-X, Xiao, T and Li, C-L 2010. Horizontal distribution of large tintinnids in the northern South China
Sea. Journal of Tropical Oceanography, 29(3): 141–150.
Fernandes, L. F. 2004. Tintinnids (Ciliophora, Tintinnina) from subtropical waters of the Southern Brazil I. Families Codonellidae,
Codonellopsidae, Coxliellidae, Cyttarocylidae, Epiplocylidae, Petalotrichidae, Ptychocylidae, Tintinnididae and Undellidae.
Revista Brasileira de Zoologia, 21(3): 551–576.
Gold, K. and Morales, E. A. 1975. Tintinnida of New York Bight: loricae of Parafavella gigantea, P. parumdentata and Ptychocylis
obtusa. Transactions of the American Microscopical Society, 94(1): 142–145.
Hada, Y. 1932a. The Tintinnoinea from Sea of Okhotsk and its neighbourhood. Journal of the Faculty of Science Hokkaido Imperial
University Series VI, 2(1): 37–60.
Hada, Y. 1932b. Report of the biological survey of Mutsu Bay. 24: The pelagic Ciliata, suborder Tintinnoinea. Science Report, Tohoku
Imperial University, 4th Series, Biology, 7: 553–573.
Hada, Y. 1937. The Fauna of Akkeshi Bay. IV: The pelagic ciliata. Journal of Faculty of Science, Hokkaido Imperial University Seris IV,
Zoology, 3: 143–216.
Hada, Y. 1938. Studies on the Tintinnoinea from the western tropical Pacific. Journal of Faculty of Science, Hokkaido Imperial
University Seris VI, Zoology, 6: 87–190.
Jiang, Y, Yang, J-P, Al-Farraj, S. A., Warren, A. and Lin, X-F 2012. Redescriptions of three tintinnid ciliates, Tintinnopsis tocantinensis,
T. radix, and T. cylindrica (Ciliophora, Spirotrichea), from coastal waters off China. European Journal of Protistology, 48(4):
314–325.
Kofoid, C. A. and Campbell, A. S. 1929. A conspectus of the marine and fresh-water ciliata belonging to the suborder Tintinnoinea: with
descriptions of new species principally from the Agassiz Expedition to the eastern tropical Pacific, 1904–1905. University of
California Press, California. 34. 403pp.
Kofoid, C. A. and Campbell, A. S. 1939. Reports on the scientific results of the expedition to the Eastern tropical Pacific, in charge to
Alexander Agassiz, by US Fish commision steamer “Albatross”, from October, 1904, to March, 1905, Lieut.-Commander LM
Garrett, USN commanding. XXXVII. The Ciliata: The Tintinnoinea, Bulletin of the Museum of Comparative Zoology of Harvard
College, Harvard.
Laval-Peuto, M. 1981. Construction of the lorica in Ciliata Tintinnina: in vivo study of Favella ehrenbergii: variability of the
phenotypes during the cycle, biology, statistics, biometry. Protistologica, 17(2): 249–272.
Lynn, D. H. 2008. The ciliated protozoa: characterization, classification, and guide to the literature. Springer, New York. 3rd ed.
Marshall, S. M. 1934. The Silicoflagellata and Tintinnoinea. British Museum, London.
Nie, D-S 1934. Notes on tintinnoinea from the Bay of Amoy. Marine Biological Association of China, Third Annual Report: 71–80.
Sharaf, G. M. 1995. On some tintinnids (Protozoa: Ciliata) from the Strait of Hormoz and the United Arab Emirates waters. Qatar
University Science Journal, 15(2): 389–398.
Souto, S. 1970. Tintinnids from the Atlantic coast between 31° and 35° south latitude (Uruguay and southern Brasil) (Protozoa, Ciliata).
Buenos Aires November 1970, Physis-Tomo XXX, no 80: 187–208.
Urrutxurtu, I. 2004. Seasonal succession of tintinnids in the Nervion River estuary, Basque Country, Spain. Journal of Plankton
Research, 26(3): 307–314.
Wang, C-C and Nie, D-S 1932. A survey of the marine protozoa of Amoy. Cont. Biol. Lab. Sci. Sco. China. Zool. Ser., 8: 285–385.
Wasik, A and Mikolajczyk, E. 1991. Discocilia (paddle cilia) in the marine ciliate Cymatocylis convallaria (Tintinnina). Cell Biology
International Reports, 15(6): 485–491.
Xu, D-P and Song, W-B 2005. Tintinnid ciliates from Qingdao (Protozoa, Ciliophora, Tintinnida). Acta Zootaxonomica Sinica, 30(3):
501–508.
Yin, K-T 1952. Primary investigation of Tintinnids in the Kiaochow Bay, Shantung, China. Journal of Shandong University, 2: 36–56.
Zhang, W, Jiang, Y, Li, J-Q, Ma, H-G and Xu, H-L 2012a. Tintinnid ciliates from coastal waters off Guangdong, with notes on three new
records of China (Protozoa, Ciliophora). Acta Hydrobiologica Sinica, 36(4): 744–750.
Zhang, W-C, Feng, M-P, Yu, Y, Zhang, C-X and Xiao, T 2012b. An illustrated guide to contemporary tintinnids in the world. Science
Press, Beijing. 499pp.
Zhao, N, Zhang, W-C, Sun, S, Song, W-B, Zhang, Y-S and Li, G-M 2007. Spatial distribution of some large tintinnids (Protozoa,
Ciliophora, Tintinnida) in Jiaozhou Bay. Oceanologia et Limnologia Sinica, 38(5): 468–475.
© Zoological Systematics, 39 (2): 372–379
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Zhang et al.
长江口海域一砂壳纤毛虫新种(纤毛门,旋毛纲)的形态学及其生境特征
张武昌 1* 丰美萍 1,2 于莹 1,2 陈旭淼 1 肖天 1
1.中国科学院海洋研究所 青岛 266071
2.中国科学院大学 北京 100049
*通讯作者:E-mail: [email protected]
摘要
在长江口海域发现砂壳纤毛虫一新种,定名为河口拟铃虫(Tintinnopsis estuariensis)
。该种壳体为不透明
黏着壳,通体覆盖矿物质颗粒,两端开口,壳体上半部分呈圆筒状,下半部分侧扁,壳体长度 120–180 μm,口径
50–75 μm,属于 Tintinnopsis 属。该种区别于同属其他相似种类的特点是壳体下半部分侧扁、下部开口为垂直开口,
口径较大。该种于 2005 年的 5 月、9 月和 11 月出现,2 月不出现,9 月丰度最大。该种出现时,水体表层温度范
围为 14–27 °C,表层盐度范围为 3.9‰–29.8‰。该种的纤毛图式、细胞及基因特征尚需进一步研究。
关键词 分类学,砂壳目,壳,新种
© Zoological Systematics, 39 (2): 372–379