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Protoraphis Simonsen, a newly recorded marine epizoic diatom genus for China
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Lang Li1, Changping Chen1, 2, *, Lin Sun3, Jiawei Zhang1, Junrong Liang1, 2, Yahui Gao1, 2, 3, *
Acta Oceanologica Sinica | 2020, 39(4) : 120 - 126
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Acta Oceanologica Sinica | 2020, 39(4): 120-126
• Marine Biology •
Protoraphis Simonsen, a newly recorded marine epizoic diatom genus for China
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Lang Li1, Changping Chen1, 2, *, Lin Sun3, Jiawei Zhang1, Junrong Liang1, 2, Yahui Gao1, 2, 3, *
Affiliations
  • 1 School of Life Sciences, Xiamen University, Xiamen 361102, China
  • 2 Key Laboratory of Ministry of Education for Coastal and Wetland Ecosystems, Xiamen University, Xiamen 361102, China
  • 3 State Key Laboratory of Marine Environmental Science, Xiamen University, Xiamen 361102, China
Published: 2020-04-25 doi: 10.1007/s13131-019-1467-z
Outline
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Epizoic diatoms on marine copepods are common in nature and may have a special ecological relationship with their hosts. However, this special ecological group is not well known, and it has only rarely been studied in the China seas. To address this knowledge gap, the species diversity and classification of epizoic diatoms on planktonic copepods were studied with samples collected from the East China Sea. In the present study, a marine araphid diatom genus Protoraphis and its type species, Pr. hustedtiana, were observed and identified by light and electron microscopy, thus representing the first record of this genus and its type species in China. This genus is characterized by a median sternum strongly bent to opposite sides and terminate in two transapical grooves at the valve ends. Protoraphis hustedtiana was found to be epizoic on the posterior body appendages and segments of the marine calanoid copepod Candacia bradyi. An internal view shows a complex, ear-shaped process that is close to the apical slit field. The ecological habitats and geographical distributions of Protoraphis were also discussed, and, together with complementary morphological studies, our results have increased the number of records for marine epizoic diatoms to three genera with three species in China, including Pseudohimantidium and Pseudofalcula.

marine epizoic diatom  /  copepod  /  Protoraphis  /  newly recorded genus  /  ear-shaped process
Lang Li, Changping Chen, Lin Sun, Jiawei Zhang, Junrong Liang, Yahui Gao. Protoraphis Simonsen, a newly recorded marine epizoic diatom genus for China[J]. Acta Oceanologica Sinica, 2020 , 39 (4) : 120 -126 . DOI: 10.1007/s13131-019-1467-z
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1 Introduction
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In the last few years, the term “epizoic diatom” has been prominent in the taxonomy of marine diatoms, and many articles on this special diatom group have been continuously published (Sar and Sunesen, 2014; Li et al., 2014; Majewska et al., 2017; Frankovich et al., 2018). Most of these studies were carried out on the carapace or neck skin of sea turtles and the exoskeleton of marine copepods (Fernandes and Calixto-Feres, 2012; Donadel and Torgan, 2016; Gárate-Lizárraga and Esqueda-Escárcega, 2018). According to their results, it seemed that epizoic diatoms occurred with greater abundance on vertebrates compared to invertebrates and that distinct differences existed in the morphology of epizoic diatoms on different hosts (Riaux-Gobin et al., 2017a, b). Numerous new diatom taxa, such as species of Tursiocola Holmes, Nagasawa & Takano, Tripterion Holmes, Nagasawa & Takano, Chelonicola Majewska, De Stefano & Van de Vijver, Poulinea Majewska, De Stefano & Van de Vijver and Medlinella Frankovich, Ashworth & Sullivan, were described from marine turtles and manatees (Frankovich et al., 2015; Majewska et al., 2015; Frankovich et al., 2016; Riaux-Gobin et al., 2017a, b; Frankovich et al., 2018). In contrast, after Hiromi et al. (1985) and Hallegraeff and McWilliam (1990) recognized only six araphid diatom taxa (Pseudohimantidium pacificum Hustedt & Krasske, Falcula hyalina Takano, Protoraphis altantica Gibson, Pr. hustedtiana var. hustedtiana Simonsen, Sceptronema orientale Takano, and Licmophora unidenticulata Takano) as epizoic diatoms on marine copepods, no new species or varieties specific to copepods have been reported.
All the araphid diatoms epizoic on marine copepods are highly distinctive, and most are either monotypic or species-poor genera. For example, both Protoraphis Simonsen and Pseudohimantidium Hustedt & Krasske have clearly visible sigmoid sternum and polar grooves under light microscopy (LM), but they can be easily distinguished by shapes (Simonsen, 1970). Falcula hyalina, which was transferred into the new genus Pseudofalcula Gómez, Wang & Lin in Gómez et al. (2018), shows two plate-like chloroplasts and arcuate valve views (Li et al., 2014). Although Pseudohimantidium pacificum possesses a sickle-like valve, it can be separated from Pseudofalcula hyalina (Takano) Gómez, Wang & Lin by its rostrate apices and stalk-forming colony (Rivera et al., 1986; Fernandes and Calixto-Feres, 2012).
Apart from Pseudohimantidium pacificum documented sixty years ago and Pseudofalcula hyalina found in the mariculture and mangrove waters, only sparse research on epizoic diatoms has been carried out in China (Voigt, 1959; Li et al., 2014). The present study describes a newly recorded epizoic diatom genus, Protoraphis, represented by Pr. hustedtiana var. hustedtiana epizoic on Candacia bradyi Scott collected from the East China Sea during a survey cruise in the autumn of 2016. Morphology and ultrastructure were examined by light and scanning electron microscopy. Biogeography and ecology of Protoraphis taxa were also briefly described.
2 Materials and methods
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2.1 Sampling
Copepods in this study were collected on October 1, 2016 by a standard zooplankton net (diameter 80 cm, mesh 505 μm) hauled vertically from the open waters in the East China Sea (26°23′58.194″N, 121°27′06.39″E) at a depth of 79 m. Samples were collected from the bottom of the net and immediately preserved in 5% seawater formalin. The East China Sea is located in the western North Pacific between China and Okinawa in the Ryukyu Arc. It is one of the largest continental shelf seas in the world (Jiao et al., 2005; Takayanagi et al., 2006). The area is about 7.5×105 km2, and the average depth is 349 m (Takayanagi et al., 2006). Three main water systems exist in the East China Sea: fresh water input from the Changjiang (Yangtze) River in the west, the Kuroshio Current in the east, and the mixing water system between them (Jiao et al., 2005). Along the shelf, picoplankton and nanoplankton are very common, and the abundance of diatoms depends on the thickness of the mixed surface layer (Takayanagi et al., 2006).
2.2 Methods
Copepods with epizoic diatoms were examined under an inverted microscope (Olympus CKX41, Japan) and then transferred into a tube with Pasteur pipettes. Epizoic diatoms were removed from the infested copepods by ultrasound at 300 W for 25 s, acidized with HCl (36%–38%) at 100°C for 20 min to eliminate organic matter, and then rinsed with distilled water eight to ten times. Cleaned material was mounted on slides and coverslips for LM (Olympus BX51, Japan) and SEM (JEOL JSM-6390LV, Japan) observations, respectively. LM micrographs were taken by a digital camera (Olympus DP71, Japan). Permanent slides were made with Naphrax® and deposited in the School of Life Sciences, Xiamen University, China.
Diatom morphological terminology, as presented in Simonsen (1970), Hallegraeff and McWilliam (1990), Sullivan (1993) and Witkowski et al. (2000), was respectively referenced.
3 Results
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Based on our observations and reports in the literature (Simonsen, 1970; Hallegraeff and McWilliam, 1990), the diatom of interest among our specimens was identified as Pr. hustedtiana var. hustedtiana, which was epizoic on the planktonic copepod C. bradyi collected from the East China Sea. This is the first record of the genus Protoraphis for China. Generic and specific descriptions follow.
3.1 Protoraphis Simonsen
Simonsen, 1970, p. 383–394, pl. 1; Gibson, 1979a, p. 109–126, Figs 1–18; Hallegraeff and McWilliam, 1990, p. 39–45, Figs 1–13; Sullivan, 1993, p. 161–167, Figs 1–8; Witkowski et al., 2000, p. 74, 75, pl. 26, Fig. 15, pl. 29, Figs 1–3.
3.1.1 Description
Cells attached to the hosts with mucilaginous stalks (Figs 1a-d). Chloroplasts two or four, large, positioned near the middle of the cell (Fig. 1d). Valves clavate to lanceolate, with broadly rounded apices (Figs 1d-f). Sternum narrow, but conspicuous, straight and median in the middle of the valve, abruptly bent to opposite sides at the ends, terminating in two polar grooves (Figs 1e, f). Transverse striae parallel, composed of rounded, elliptical or rectangular areolae, interrupted by the sternum (Figs 2a, b, e). Apical groove surrounded by a hyaline zone, penetrating the frustule, forming a siliceous rim (basis) and protruding as a series of specific structures internally (Figs 2b-d and 3b-d). Apical slit fields starting on the valve face and going down the mantle with unequal vertical openings (Figs 2a-d). Girdle bands several to numerous, perforated by two rows of rounded or elongate pores per band (Fig. 2f).
3.1.2 Ecology
Protoraphis was established by Simonsen in 1970. Up to now, only two species and one variety have been reported. All taxa inhabit marine environments and most of them are epizoic on copepods, snails or the second stage larva of a barnacle, the Cypris (Foged, 1984; Sullivan, 1993; Gómez et al., 2018).
3.2 Protoraphis hustedtiana var. hustedtiana Simonsen
Simonsen, 1970, p. 383–394, pl. 1; Hallegraeff and McWilliam, 1990, p. 39–45, Figs 1–13; Witkowski et al., 2000, p. 75, pl. 29, Figs 1 and 2; Guiry and Guiry, 2018.
3.2.1 Description
Chloroplasts four, large, positioned close to the middle of the cell (Figs 1b-d). Frustules in girdle view rectangular to slightly inflexed (Fig. 1d). Valves lanceolate, diagonally symmetrical, with broadly rounded apices (Figs 1d-f and 2a). Apical axis 45–129 μm, transapical axis 4–10 μm. Striae uniseriate, composed of rounded areolae (Figs 2a-e). Transverse rows 31 in 10 μm, longitudinal rows 3–4 in 1 μm. Sternum distinct, linear, lying in the median position for almost its entire length, bent to opposite sides at the apices (Figs 1e, 1f and 2a-d). A total of 12–16 vertical openings present in the apical slit fields (Figs 2b-d). A groove (1.1–1.7 μm long) penetrating the valve located in the hyaline zone at the end of sternum, exposing a siliceous structure concave to the valve pole (Figs 2a-d). Internally, margin of groove thickened and developed as an ear-shaped basis (1.3–2 μm long), with a large E-shaped lip protruding from the distal side and a small lamelliform or U-shaped lip projecting from the opposite side (Figs 3b-d). Transapical striae slightly depressed between weakly developed virgae (Fig. 3e). Girdle bands open, with two rows of rounded pores (Fig. 2f).
3.2.2 Ecology
In our material, Pr. hustedtiana var. hustedtiana attached to the hosts with unbranched mucilaginous stalks. They usually occurred as solitary cells or formed short chains by apex-to-apex. It seemed that this taxon preferred to infect the posterior body appendages and segments of the calanoid copepods. All three host copepods in our study were males. Hallegraeff and McWilliam (1990) also reported that the diatom taxon was only epizoic on male calanoid copepods (C. discaudata Scott).
3.2.3 Distribution
The diatom species Pr. hustedtiana was first found in the Arabian Sea and Persian Gulf by Simonsen in 1970. Hallegraeff and McWilliam (1990) recorded Pr. hustedtiana, which was recognized as var. hustedtiana in Sullivan (1993), from coastal waters of northwestern Australia. Our copepods infested with diatoms were sampled from open waters in the East China Sea.
4 Discussion
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Protoraphis is a distinct araphid diatom genus characterized by its linear valve, sigmoid sternum and transapical grooves at the valve ends. Its type species, Pr. hustedtiana, was first described in Simonsen (1970). After that, Gibson (1979a) reported a new species, Pr. atlantica, from the northwestern Atlantic Ocean. In addition, a variety, Pr. hustedtiana var. nana Takano, was reported from the northwestern Pacific Ocean (Takano, 1985). Results showed that its transapical groove was shorter than that in the nominate variety and that an internal Y-shaped process was positioned at the groove. The fine structure of Pr. hustedtiana var. hustedtiana was first revealed by Hallegraeff and McWilliam (1990). Considering that the ear-shaped processes located near the apices were complex and specific, the authors hypothesized that the raphe system in raphid diatoms and the grooves in Pr. hustedtiana var. hustedtiana were homologous. Pseudohimantidium also displays similar sternum and grooves, but it can be easily distinguished by its scythe-shaped valve and series of rimoportulae at each apex of the valve (Simonsen, 1970; Rivera et al., 1986). Based on these facts, the two genera were merged into the family Protoraphidaceae by Simonsen (1970). So far, although the significance of the groove has not been confirmed, most studies have recognized that the mucilaginous stalks in Protoraphidaceae taxa are not secreted by this structure (Gibson, 1979a, b; Sullivan, 1993).
Protoraphis has some morphological similarities with Neosynedra Williams & Round, Cyclophora Castracane and Lucanicum Lobban & Ashworth (Table 1). All of these diatoms share somewhat lanceolate or linear valve outlines and structureless valves when observed with light microscope. Since an apical slit field is one of their common features, several studies have reported on this feature, making respective comparisons among these genera (Round et al., 1990; Lobban and Ashworth, 2014; Gómez et al., 2018). The Protoraphis taxa differ mainly from N. provincialis (Grunow) Williams & Round by their grooves with complex labiate processes and uninterrupted apical slits (Table 1). Cyclophora is characterized by the central pseudosepta on the valves and the absence of polar grooves. The general shape of this genus is often constricted in the middle or below the apices (Ashworth et al., 2012). Lucanicum is a benthic genus with long chains, while Protoraphis can only form short chains or live in a solitary frustule. Like Neosynedra and Cyclophora, Lucanicum also bears a simple rimoportula near each apex (Table 1). The striae of Lucanicum are composed of transapically elongated macroareolae, while areolae in Protoraphis are very small (Lobban and Ashworth, 2014). Consequently, critical features of these genera are apparent and easily to be recognized under light and electronic microscopy.
The dimensions and fine structures of the valves in our material are close to those in Hallegraeff and McWilliam (1990) (Table 2). But our SEM images revealed that the U-shaped lip combined with the groove can develop as a lamelliform structure with two spines (Fig. 3b). Compared to the complex ear-shaped labiate process in Pr. hustedtiana var. hustedtiana, a simpler Y-shaped protrusion presents in var. nana (Sullivan, 1993). Sullivan (1993) suggested that “all features of valve morphology appear to be identical” in the genus Protoraphis. In fact, some slight distinctions in valve morphology are present within the genus, except for the heteropolarity of Pr. atlantica. It is clear that the maximum valve lengths in both Pr. hustedtiana var. nana (57 μm) and Pr. atlantica (50 μm) are much shorter than valve length in Pr. hustedtiana var. hustedtiana (130 μm). According to Figs 4–8 in Sullivan (1993), the areolae in Pr. hustedtiana var. nana, which are similar to those in Pr. atlantica, seem to be elliptical or rectangular. However, Pr. hustedtiana var. hustedtiana only has small, rounded areolae based on our results (Figs 2b-e and 3b-e) and those of Hallegraeff and McWilliam (1990). Furthermore, both Pr. hustedtiana var. nana (Fig. 4 in Sullivan, 1993) and Pr. atlantica (Fig. 4 in Gibson, 1979a) have two rows of elongate pores on the girdle bands, while the bands of Pr. hustedtiana var. hustedtiana are pierced by two rows of rounded pores (Fig. 2f). Therefore, although no internal view of Pr. hustedtiana was shown in Gómez et al. (2018), the taxon seems rather to represent var. nana based on their description.
Up to now, Protoraphis has been reported from the Arabian and Persian Gulfs, the United States, Japan, Australia, the Caribbean Sea, Brazil and the East China Sea (Simonsen, 1970; Gibson, 1979a; Foged, 1984; Takano, 1985; Hallegraeff and McWilliam, 1990; Sullivan, 1993; Witkowski et al., 2000; Gómez et al., 2018). This genus distributes mainly in the Indian Ocean, the West Atlantic Ocean and the North Pacific Ocean. Our result enlarges the global distribution of this genus and indicates that Protoraphis may be widespread in the world. In the present study, Pr. hustedtiana var. hustedtiana was observed on the posterior body appendages and segments of planktonic copepods, consistent with the results in Gibson (1979a) and Hallegraeff and McWilliam (1990). Candacia Dana seemed to be one of the most common copepod hosts for Protoraphis. The occurrence of Protophis taxa (except for Pr. hustedtiana var. nana and Pr. hustedtiana f. latior Foged) on specific body parts is probably related to the motion of planktonic copepods. As the main appendages for swimming, the first antennae of calanoid copepods are generally longer than those of harpacticoid families, and their strong swing may interfere with the attachment of epizoic diatoms to the anterior body appendages and segments. But harpacticoid copepods are mostly benthic and their first antennae are usually very short. The less swing range of first antennae may have no influence on the attachment diatoms. That may explain why Pr. atlantica can be found on the all body segments of harpacticoid copepods (Gibson, 1979a). In some ways, the infestation of S. orientale on the harpacticoid copepod Euterpina acutifrons Dana confirmed our inference of the first antennae (Skovgaard and Saiz, 2006; Sar and Sunesen, 2014). As for Pseudofalcula hyalina, which attaches itself to various parts of Acartia Dana by mucilaginous pads (Takano, 1983; Prasad et al., 1989), its smaller cell size and shorter extension may not interfere with movement of the first antennae. Gibson (1979a) insisted that the infestation of Pr. atlantica can be related to the mating behavior of copepod hosts. However, neither our observations nor those of Hallegraeff and McWilliam (1990) were based on finding Pr. hustedtiana var. hustedtiana on female copepods. In our opinion, more specimens from different locations should be examined to confirm if Pr. hustedtiana var. hustedtiana is specific to male individuals, and more in vitro experiments should be conducted to explain the relationship between Pr. hustedtiana var. hustedtiana and Candacia.
Acknowledgements
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We thank Caiming Wu and Luming Yao from the Electron Microscopy Laboratory, Xiamen University, for providing assistance with SEM observation. We also thank David Martin for his assistance with language editing.
Funding
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  • The National Key Research and Development Program of China under contract No. 2016YFA0601302; the National Natural Science Foundation of China under contract Nos 41876146 and 41476116.
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doi: 10.1007/s13131-019-1467-z
  • Receive Date：2018-12-16
  • Online Date：2026-03-31
  • Published：2020-04-25
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  • Received：2018-12-16
  • Accepted：2019-04-22
Funding
The National Key Research and Development Program of China under contract No. 2016YFA0601302; the National Natural Science Foundation of China under contract Nos 41876146 and 41476116.
Affiliations
    1 School of Life Sciences, Xiamen University, Xiamen 361102, China
    2 Key Laboratory of Ministry of Education for Coastal and Wetland Ecosystems, Xiamen University, Xiamen 361102, China
    3 State Key Laboratory of Marine Environmental Science, Xiamen University, Xiamen 361102, 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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