Mar Biodiv DOI 10.1007/s12526-016-0607-x
CCZ BIODIVERSITY
Species diversity of dinophysoid dinoflagellates in the Clarion–Clipperton Fracture Zone, eastern Pacific Carmen Zinssmeister 1 & Tanja Wilke 2 & Mona Hoppenrath 1,2
Received: 30 March 2016 / Revised: 25 October 2016 / Accepted: 14 November 2016 # Senckenberg Gesellschaft für Naturforschung and Springer-Verlag Berlin Heidelberg 2016
Abstract Species diversity of dinophysoid dinoflagellates is especially high in subtropical and tropical oceans. Only a few studies about the diversity of these dinoflagellates exist from the eastern Pacific. The offshore, subtropical Clarion– Clipperton Fracture Zone (CCZ), in the eastern part of the Pacific between Mexico and Hawaii, is an area of interest for deep sea manganese nodule mining. Therefore, geological research is ongoing, but also biodiversity research from the deep sea up to the surface is of importance. This study adds to the biodiversity knowledge by describing dinophysoid dinoflagellates in the area for the first time. Phytoplankton samples were collected during two cruises to the CCZ, MANGAN 2013 (April and May 2013) and ABYSSLINE AB01 (October 2013), and investigated morphologically. Sixty-six species of dinophysoid dinoflagellates were found and documented by light and scanning electron microscopy. These species belonged to 11 genera: Amphisolenia F.Stein (9), Citharistes F.Stein (1), Dinophysis Ehrenb. (15), Histioneis F.Stein (8), Latifascia sp. (1), Metaphalacroma L.S.Tai (1), Parahistioneis Kof. & Skogsb. (3), Phalacroma F.Stein (16), Pseudophalacroma Jørg. (2), Ornithocercus F.Stein (9) and Triposolenia Kof. (1). Seven of the taxa, Amphisolenia sp. 1 a n d 2 , P h a l a c ro m a s p . 1 , D i n o p h y s i s s p . 1, Communicated by C. Smith * Carmen Zinssmeister
[email protected]
1
German Center for Marine Biodiversity Research (DZMB), Senckenberg am Meer, Südstrand 44, 26382 Wilhelmshaven, Germany
2
IBU—Institut für Biologie und Umweltwissenschaften, Carl von Ossietzky Universität Oldenburg, Carl-von-Ossietzky-Str. 9–11, 26129 Oldenburg, Germany
Pseudophalacroma sp. 1, Histioneis spec. and cf. Latifascia spec., could be identified only to the genus level and may represent new species. This diversity was unexpected compared to the available open ocean records for the eastern Pacific (14 species, four genera). Almost half the number of species recorded before in the eastern Pacific (including coastal samples) was observed, corresponding to about one-fifth of the known dinophysoid diversity. Keywords Dinophysales . Morphology . Amphisolenia . Citharistes . Dinophysis . Histioneis . Latifascia . Metaphalacroma . Parahistioneis . Phalacroma . Pseudophalacroma . Ornithocercus . Triposolenia
Introduction Dinoflagellates are a diverse group of protists concerning morphology and life styles, with over 2000 described species (Hackett et al. 2004; Hoppenrath 2016; Taylor et al. 2008). About 300 of all accepted species names belong to the thecate dinophysoid dinoflagellates (Gómez 2012). They are morphologically characterised by their special theca construction with sagittal suture (dinophysoid tabulation with highly conserved thecal plate pattern with six or seven epithecal, four cingular, four sulcal and four hypothecal plates, with two large lateral epithecal and hypothecal plates dominating the theca; see e.g. Figs. 3 and 5) and classified within the order Dinophysales (Fensome et al. 1993; Hoppenrath 2016; Kofoid and Skogsberg 1928). The spelling Dinophysales (instead of Dinophysiales) is used following P.C. Silva’s recommendation in Gómez et al. (2011, Appendix S1). They compromise 16 genera (Table 3): Amphisolenia F.Stein, Citharistes F.Stein, Dinofurcula Kof. & Skogsb, Dinophysis Ehrenb., Histioneis F. Stein, Histiophysis Kof. & Skogsb., Latifascia Loebl. &
Mar Biodiv
A.R. Loebl, Metadinophysis D.S.Nie & Chia C.Wang, Metaphalacroma L.S.Tai & Skogsb., Ornithocercus F.Stein, Parahistioneis Kof. & Skogsb., Phalacroma F.Stein, Proheteroschisma L.S.Tai & Skogsb., Pseudophalacroma Jørg., Sinophysis D.S.Nie & Chia C. Wang and Triposolenia Kof (Gómez 2012). The most species-rich dinophysoid genera are Dinophysis with 78, Phalacroma with 69 and Histioneis with 52 described species. The highest species diversity can be found in marine subtropical and tropical oceanic (planktonic) habitats (Kofoid and Skogsberg 1928; Okolodkov 2014). These mainly heterotrophic taxa occur in low cell abundance in an unknown depth between the water surface and about 200 m. So far, all dinophysoid genera are planktonic, except the benthic genus Sinophysis with seven species (Hoppenrath 2000; Hoppenrath et al. 2013). Pioneering work on dinophysoids has been done by C. A. Kofoid, J. R. Michener, T. Skogsberg and L.-S. Tai, who described 88 new species and five new genera based on plankton samples from coastal and oceanic regions along the eastern Pacific (Kofoid and Michener 1911; Kofoid and Skogsberg 1928; Tai and Skogsberg 1934). They investigated material from an expedition with the U.S. Fish Commission Steamer ‘Albatross’ (under the leadership of Alexander Agassiz from October 1904 to March 1905) and documented 132 species in total belonging to 11 genera of dinophysoid dinoflagellates (Kofoid and Skogsberg 1928). Since then, there has not been intensive sampling in the area. Further studies focused exclusively on coastal regions such as the tropical Mexican Pacific (Esqueda-Lara et al. 2013; Okolodkov and Gárate-Lizárraga 2006). Forty-one species in five genera (Amphisolenia, Dinophysis, Histioneis, Metaphalacroma, Ornithocercus) were recorded by Hernández-Becerril et al. (2008) and 34 species in four genera (Amphisolenia, Dinophysis, Histioneis, Ornithocercus) by Esqueda-Lara and Hernández-Becerril (2010). Thirty-three species of Dinophysis have been documented from the central and western Pacific (Nguyen et al. 2008). Omura et al. (2012) recorded 93 species within 11 genera, including 36 Dinophysis species, in the western Pacific. Phalacroma has been synonymised with Dinophysis in these accounts (Nguyen et al. 2008; Omura et al. 2012). Seventeen species of Histioneis (including Parahistioneis) were documented from the western Pacific (Gómez 2005). The Atlantic Ocean, especially the Gulf of Mexico, is the best studied area concerning dinophysoid diversity (EsquedaLara et al. 2013; Licea et al. 2004; Okolodkov 2014; ParraToriz et al. 2014; Steidinger et al. 2009). Between 2005 and 2008, Okolodkov (2014) documented 38 species within eight genera (Amphisolenia, Dinophysis, Heteroschisma, Histioneis, Ornithocercus, Phalacroma, Pseudophalacroma, Sinophysis ) and 50 species within seven genera (Amphisolenia, Dinophysis, Heteroschisma, Histioneis, Ornithocercus, Metaphalacroma, Triposolenia) were
recorded by Licea et al. (2004). Heteroschisma nom. rej. should no longer be used; instead, Latifascia nom. cons. is available (Silva 1994). Steidinger et al. (2009) summarised all known records of dinoflagellates and listed 172 dinophysoid species from the Gulf of Mexico. In the coastal waters of Brazil, 43 Dinophysales species were identified (Haraguchi and Odebrecht 2010). Off the east coast of the USA, Marshall (1976) recorded the diversity of phytoplankton and listed 33 dinophysoid species within five genera. The Clarion–Clipperton Fracture Zone (CCZ), part of the eastern Pacific Ocean, has not been a site for dinophysoid research. To the best of our knowledge, only one study on Clipperton Island, a coral atoll in the northeastern Pacific Ocean at the eastern border of the CCZ, described peridinoid dinoflagellates (Couté et al. 2012). The closest known site to the CCZ investigated by phytoplankton taxonomists has been at least 850 km south-eastward, about 100 years ago (Kofoid and Skogsberg 1928). The present study contributes to the knowledge of dinoflagellate biodiversity in the open eastern Pacific Ocean, especially to the dinophysoid species diversity, and it adds to their biogeographic ranges.
Materials and methods Water samples have been collected during the ABYSSLINE AB01 and MANGAN 2013 cruises from the CCZ between Hawaii and the USA coast (Fig. 1). All three samples A–C of the ABYSSLINE AB01 cruise have been taken at the same station D, UK1 – stratum A (13°57′797 N, 116°34′095 W) on October 15, 2013. The distance from this sampling area to the MANGAN 2013 locations was about 240 km southward. MANGAN 2013 samples have been collected at two parts at German Mn-nodule license areas of the CCZ (Table 1). Plankton sample numbers 1–20 have been taken at the eastern German Mn-nodule license areas between April 17 and April 19 and sample numbers 21–29 have been collected about 50 km westwards between May 1 to 3, 2013. During the MANGAN 2013 cruise, the samples were achieved through different collecting techniques and mesh sizes (Table 1). First, these included hauls with two different plankton nets after Apstein (Hydro-Bios, Kiel, Germany). Six vertical plankton samples (numbers 4, 8 11, 14, 17 and 20) were taken with a 80-μm mesh size and three (numbers 23, 26 and 29) with a 20-μm mesh size from 150 m depth. Therefore, the net was weighted. Surface plankton samples were taken six times (numbers 2, 7, 10, 13, 16 and 19) with the 20-μm mesh size net and five times (numbers 3, 6, 22, 25 and 28) with the 80-μm mesh size nets. Additionally, seawater was conveyed nine times (numbers 1, 5, 9, 12, 15, 18, 21, 24 and 27) by a water pump filtration through a 20-μm sieve. Later on during the ABYSSLINE AB01 cruise, three water pump-filtrated samples (A–C within station list, Table 2) were taken through a mesh
Mar Biodiv Fig. 1 Map showing the eastern Pacific with Hawaiian islands and the American coast at the right map side. Sampling areas of the ABYSSLINE AB01 and MANGAN 2013 cruises are marked with arrows between the Clarion and Clipperton Fracture Zones. The dotted lines show the research vessel ‘Albatross’ expedition areas from 1904 to 1905 (Kofoid and Skogsberg 1928). Investigated stations near to the Clarion–Clipperton Fracture Zone (CCZ) are st. 4540–4545
size of 20 μm. All plankton samples were fixed within acid Lugol solution at a dilution of 1 ml Lugol solution to 100 ml
Table 1
sample and stored in light-proof bottles at room temperature until investigations were performed.
MANGAN 2013 sampling data. List of sample numbers, station name, coordinates, sampling method, date and time
No.
Station
Latitude °N
Longitude °W
1 2 3 4 5
KM13-PN35 KM13-PN35 KM13-PN35 KM13-PN35 KM13-PN38
11°51.683′ 11°51.683′ 11°51.683′ 11°51.683′ 11°51.456′
117°00.367′ 117°00.367′ 117°00.367′ 117°00.367′ 117°01.355′
6 7 8 9 10
KM13-PN38 KM13-PN38 KM13-PN38 KM13-PN40 KM13-PN40
11°51.456′ 11°51.456′ 11°51.456′ 11°51.269′ 11°51.269′
117°01.355′ 117°01.355′ 117°01.355′ 117°02.379′ 117°02.379′
11 12
KM13-PN40 KM13-PN43
11°51.269′ 11°49.398′
117°02.379′ 117°01.937′
13 14
KM13-PN43 KM13-PN43
11°49.398′ 11°49.398′
117°01.937′ 117°01.937′
15 16 17 18 19 20 21 22 23 24 25 26 27 28 29
KM13-PN45 KM13-PN45 KM13-PN45 KM13-PN47 KM13-PN47 KM13-PN47 KM13-PN82 KM13-PN82 KM13-PN82 KM13-PN87 KM13-PN87 KM13-PN87 KM13-PN92 KM13-PN92 KM13-PN92
11°49.659′ 11°49.659′ 11°49.659′ 11°49.879′ 11°49.879′ 11°49.879′ 11°48.002′ 11°48.002′ 11°48.002′ 11°47.425′ 11°47.425′ 11°47.425′ 11°49.607′ 11°49.607′ 11°49.607′
117°00.817′ 117°00.817′ 117°00.817′ 116°58.710 116°58.710 116°58.710 117°30.656′ 117°30.656′ 117°30.656′ 117°32.725′ 117°32.725′ 117°32.725′ 117°30.919′ 117°30.919′ 117°30.919′
Vertical (μm)
Surface (μm)
Filtered (μm)
Date 2013 (UTC)
Time (UTC)
20 < 100
17. Apr. 17. Apr. 17. Apr. 17. Apr. 17. Apr.
15:34–18:07 17:20–17:30 17:33–17:43 14:24–15:18 23:54–3:37
17. Apr. 17. Apr. 17. Apr. 18. Apr. 18. Apr.
00:06–00:16 00:16–00:27 23:51–0:53 4:56–8:45 6:09–6:19
18. Apr. 18. Apr.
5:06–6:00 15:04–18:53
18. Apr. 18. Apr.
14:57–15:07 14:28–15:42
18. Apr. 18. Apr. 18. Apr. 19. Apr. 19. Apr. 19. Apr. 01. May 01. May 01. May 02. May 02. May 02. May 03. May 03. May 03. May
20:07–23:56 19:53–20:03 19:54–20:38 01:34–5:23 10 min 1:10–2:12 1:03–4:06 1:05–1:15 1:01–2:07 22:45–1:53 22:42–22:52 22:34–23:57 19:33–23:27 19:07–19:17 19:02–20:01
20 80 80 20 < 100 80 20 80 20 < 100 20 80 20 < 100 20 80 20 < 100 20 80 20 < 100 20 80 20 < 100 80 20 20 < 100 80 20 20 < 100 80 20
6b, c – 6d 6e 6g 6f 6a 6h 3m/2l – – 2g, l/3e 2o, 3g 2n, 3f
Amphisolenia bidentata Schröder Amphisolenia cf. lemmermanni Amphisolenia schauinslandii Lemmerm. Amphisolenia palmata F.Stein Amphisolenia cf. palmata Amphisolenia palaeotheroides Kof. Amphisolenia sp. 1 Amphisolenia sp. 2 Amphisolenia thrinax F.Schütt Citharistes regius F.Stein Dinophysis acuta Ehrenb. Dinophysis cf. caudata Dinophysis exigua (Kof. & J.R. Michener) Balech Dinophysis expulsa Kof. & J.R.Michener Dinophysis cf. fortii D. hastata group: - D. hastata F. Stein - D. cf. phalacromoides - D. cf. uracanthoides - D. pusilla Jørg. - D. schuetii G. Murray & Whitting Dinophysis lativelata (Kof. & J.R.Michener) Balech Dinophysis infundibula F. Schütt Dinophysis similis Kof. & Skogsb. Dinophysis cf. punctata Dinophysis sp. 1 Histioneis alata Rampi Histioneis biremis F.Stein Histioneis cf. costata Histioneis cf. crateriformis Histioneis elongata Kof. & J.R.Michener Histioneis longicollis Kof. Histioneis striata Kof. & J.R.Michener Histioneis sp. (similar H. costata) Cf. Latifascia Metaphalacroma skogsbergii L.S. Tai Ornithocercus formosus Kof. & J.R.Michener Ornithocercus heteroporus Kof. Ornithocercus magnificus F.Stein Ornithocercus quadratus f. assimilis Kof. & Skogsb. Ornithocercus quadratus f. quadrata F.Schütt Ornithocercus splendidus F. Schütt Ornithocercus skogsbergii Abé Ornithocercus steinii F.Schütt Ornithocercus thumii (Schmidt) Kof. & Skogsb. Parahistioneis cf. para 2a, e, i/3a 2d/3c 2h 2c 2b/3b 2f/3d 2k/3j 2j 2m/3h 2i 8g 8h 8j 8e 8f 8i 8d – 5d 3l/2p – 7f 7e 7c 7a 7d 7b 7g 7h 8b
Figs
Taxa
x x
x
x x x
x x x
x
x
x
x
x x x x x
1
x x x x x x x x x
x
x
x
x x x
x
x
x
x
x
2
x x
x
x x x
x
x
x
x
x x x x x x
x x x x
x x
x
3 4 5
x x x x
x x x x x x x
x
x
x
x
x
x x x x
x
x
x
x
6 7
x
x
x x
x
x
x
x x x x
x x x x x x
x
x x
8 9
x x x
x x x
x
x x
x x x x
x
x
x
x
x x
x
x x
x x x
x
x x
x
x
x
x
x
x x
x x x x
x
x x
x
x x
x
x
x x
x x
x
x
x
x x
x
x x x
x
x
x
x
x
x
x x
x x x
x x x
x
x
x
x
x
x x
x
x x
x
x x x
x
x x x
x
x x
x x x
x x x x
x
x x x
x x
x x
x
x x
x x
x
x x
x x x
x
x x x x
x
x x
x
x
x x
x
x
x x
x x x x x
x
x
x
x
x
x x
x
x x
x x x
x
x
x
x
x
x x
x
x
x
x
x
x
x x x x
x
x x
x
x x
x
x x
x x
x x
x x x
x
x x x
x
x x
x x
x
x
x x
x
x x x
x
x
x
x
x x x x x x
x x x
x
x
x x x
x x
x
x x x x x x x x
x
x
x
10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 A B C
18 2 3 3 2 1 1 2 2 13 1 1 19 6 2 0 17 4 5 4 5 20 12 11 3 1 1 5 1 1 7 6 1 3 1 3 1 20 20 22 14 12 2 32 31 2
∑
Table 2 Taxa found and their occurrence within the samples of the CCZ. MANGAN 2013 cruise sample numbers 1–20 western collecting area, 21–29 eastern collecting area and ABYSSLINE AB01 cruise A–C. ∑ horizontal: number of samples in which the species has been found; ∑ vertical: number of all species within a sample
Mar Biodiv
Figs 8a 8c 4c/5c 4o 4j/5m 4h/5h 4i/5l 4b/5b 4f/5g 4l/5h 4g/5e 4m 4n/5i 5j, k 4a/5a 4e/5f – 4c 3k/2r 2q 6i
Taxa
Parahistioneis paraformis Kof. & Skogsb. Parahistioneis cf. pieltainii Phalacroma amandula (Balech) Sournia Phalacroma apicatum Kof. & Skogsb. Phalacroma argus F.Stein Phalacroma capitulata Balech Phalacroma cuneus F.Schütt Phalacroma doryphorum F. Stein Phalacroma favus (Kof. & J.R.Michener) Abé Phalacroma hindmarchii G.Murray & Whitting Phalacroma mitra F.Schütt Phalacroma operculoides F. Schütt Phalacroma parvulum F.Schütt Phalacroma cf. parvulum Phalacroma porodictyum F.Stein Phalacroma rapa F. Stein Phalacroma cf. rotundata Phalacroma sp. 1 Pseudophalacroma nasutum (F.Stein) Jørg. Pseudophalacroma sp. Triposolenia bicornis Kof.
Table 2 (continued)
x x
x x
x x
x x x
x
x
8 9
x x x x x x
x
x x x x
x
x
x
x
x
x
x
x
x
x
x
x x
x
x
x x x
x
x
x
x x
x
x x
x x
x
21 20 10 22 22 3
x x
x x
x x
x
x
x x x
x
x x
x x
24 20 6
x
x x x
x
x x x x
x
26 4
x x
x
x x x x x x x
x
9
x
x
8
x
x
x
3
x
x
x
x
x 14 17 7
x
x
x
x
5
x
x x x x
x x x x
x x
x
x x x
x x x
x
24 32 24
x x x
x x x x
x
1 1 16 4 10 7 12 19 14 5 14 1 12 7 9 9 1 10 12 2 1
10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 A B C ∑
29 31 8 5 21 5 26 7 22 30 5
x
x x x x
x
x x x
x
x
x
x
x
x x x
x
6 7
x
x x x x x
x x x
x
x x x
x
3 4 5
x
x x x
2
x x x
1
Mar Biodiv
Mar Biodiv
Dinophysales species were isolated and documented at a 400× magnification with an inverted microscope (LEICA DM IL) equipped with a digital camera (LEICA DFC290, software LAS v3.6). For scanning electron microscopy (SEM), isolated cells were transferred on a 5-μm TMTP Isopore™ membrane filter connected with a syringe and carefully washed at least five times with distilled water. Afterwards, membrane filters were air-dried, fixed on an SEM stub and sputter-coated with gold/palladium (BAL-TEC SCD 050 Sputter Coater). SEM pictures were taken with two different microscopes: a Hitachi S-3200N SEM at a voltage of 20 kV equipped with an SE (secondary electron detector) and a Tescan VEGA3 SEM at a voltage of predominantly 10 and 15 kV using an SE, BSE (backscatter electron detector) or both detectors in combination. Pictures and cell measurement were processed with Adobe Photoshop CS6, version 13.0.1 × 64. Documented dinophysoid dinoflagellate cells were morphologically characterised including data about thecal details like their outline in lateral view (cell shape), cell size and micromorphology of cingular and sulcal lists, additional appendages and thecal ornamentation. For identification, the following literature was used: Abé (1967a, b), Esqueda-Lara et al. (2013), Gómez (2005), Gómez et al. (2008), Haraguchi and Odebrecht (2010), Ojeda (1999), Jensen and Daugbjerg (2009), Jørgensen (1923), Kofoid and Michener (1911), Kofoid and Skogsberg (1928), Le et al. (2012), Nguyen et al. (2008), Okolodkov (2014), ParraToriz et al. (2014), Schiller (1933), von Stein (1883) and Tai and Skogsberg (1934). The genera Phalacroma and Dinophysis were separated based on the height of the epitheca and the orientation of cingular lists (Jensen and Daugbjerg 2009; Kofoid and Skogsberg 1928; von Stein 1883). Species with hardly or clearly visible epitheca and horizontal cingular lists were placed into Phalacroma. Contrary to Phalacroma, the epitheca of Dinophysis species was not visible and at least the upper cingular list was orientated upwards (funnel-shaped). Histioneis was distinguished from Parahistioneis by the presence of a cross-rib on the postcingular list and a cingulum decidedly wider dorsally.
Results In total, 66 dinophysoid species were recorded from the CCZ (Table 2, Figs. 2, 3, 4, 5, 6, 7 and 8). These species have been identified as belonging to 11 different genera. Samples 1–20 from the more eastern sampling areas (Fig. 1) included 58 species, samples 21–29 from the westward area (Fig. 1) included 38 species and samples A–C of the ABYSSLINE AB01 cruise (Fig. 1) included 38 species (Table 2). The species composition of the single samples is summarised in Table 2. Nine species of Amphisolenia (Fig. 6), one species of Citharistes (Figs. 2 and 3), 15 species of Dinophysis (Figs. 2 and 3), eight species of Histioneis (Fig. 8), one species of cf. Latifascia (Fig. 5d), one
species of Metaphalacroma (Figs. 2 and 3), nine species of Ornithocercus (Fig. 7), three species of Parahistioneis (Fig. 8), 16 species of Phalacroma (Figs. 4 and 5), two species of Pseudophalacroma (Figs. 4 and 5) and one Triposolenia species (Fig. 6i) were documented. In addition to the documented species (Figs. 2, 3, 4, 5, 6, 7 and 8), Amphisolenia sp. 2, Dinophysis acuta Ehrenb., Ornithocercus formosus Kof. & J.R.Michener and Phalacroma cf. rotundata were observed. Seven species (Amphisolenia sp. 1 and 2, Phalacroma sp., Dinophysis sp., Pseudophalacroma sp., Histioneis sp. and cf. Latifascia sp.) could not be identified yet. The amount of cells of most taxa was low and some species were represented at just one station through one cell, namely Amphisolenia palaeotheroides (Fig. 6f), Amphisolenia sp. 1 (Fig. 6a), Dinophysis acuta (not shown), Dinophysis cf. caudata (not shown), Dinophysis sp. 1 (Fig. 2i), Histioneis cf. crateriformis (Fig. 8e), cf. Latifascia sp. (Fig. 5d), Ornithocercus formosus (not shown), Phalacroma operculoides F. Schütt (Fig. 4m), Phalacroma sp. 1 (Fig. 4k) and Triposolenia bicornis Kof. (Fig. 6i). On the other hand, some species were quite common and were found at all three sampling areas (Table 2). One species, Ornithocercus steinii F.Schütt (Fig. 7g), was present in all samples (Table 2). Species occurring in the majority of samples were Amphisolenia bidentata Schröder (Fig. 6b, c), Dinophysis exigua (Kof. & J.R.Michener) Balech (Figs. 2g, l and 3e), Dinophysis hastata F.Stein (Figs. 2a, e and 3a), Dinophysis lativelata (Kof. & J.R.Michener) Balech (Figs. 2f and 3d), Ornithocercus thumii F.Schütt (Fig. 7h), Ornithocercus quadratus f. assimilis (Fig. 7c), Ornithocercus magnificus F.Stein (Fig. 7i), Ornithocercus heteroporus Kof. (Fig. 7f) and Phalacroma doryphorum F. Stein (Figs. 4b and 5b). The most species-rich samples with 30 or more species were 2, 10 and B, and the lowest species composition was documented within samples 17 and 25 (Table 2). Species quantification was out of the scope of the present study. Only a relative trend in abundances and composition of taxa was recognised. Dinophysis exigua and D. lativelata were frequently observed in MANGAN 2013 samples in high cell numbers compared to other taxa. High cell numbers of the larger species Dinophysis hastata, Phalacroma porodictyum F.Stein and Phalacroma doryphorum F.Stein were present in ABYSSLINE AB01 2013 samples.
Discussion Past work on dinophysoid dinoflagellate diversity from the eastern tropical Pacific was done at the beginning of the 20th century by C.A. Kofoid and T. Skogsberg. They recorded and described 132 species in detail, including 11 genera (Kofoid and Skogsberg 1928). These genera were also documented in the present study (Table 3), except for Dinofurcula. Three species were documented in the CCZ, which were not recorded in the eastern Pacific before. They belonged to the
Mar Biodiv
Fig. 2 Light micrographs of Dinophysis, Pseudophalacroma, Metaphalacroma and Citharistes species. a, e, i D. hastata; b D. schuetti; c D. pusilla; d D. cf. phalacromoides; e D. hastata; f D. lativelata; g D. exigua; h D. cf. uracanthoides; i D. sp. 1; j
D. similis; k D. infundibula; l D. exigua; m D. cf. punctata; n D. cf. f o r t i i ; o D . e x p u l s a ; p M e t a p h a l a c ro m a s k o g s b e rg i i ; q Pseudophalacroma sp.; r Pseudophalacroma nasutum; s Citharistes regius. All to scale, bar = 10 μm
Mar Biodiv
Fig. 3 Scanning electron microscopic pictures, all to the same scale of 10 μm. Thecal plates H2 and H3 (hypotheca plates 2 and 3), E3 (epitheca plate 3). a Dinophysis hastata; b D. schuetti; c D. cf. phalacromoides; d
D. lativelata; e D. exigua; f D. cf. fortii; g D. expulsa; h D. cf. punctata; i, j D. infundibula; k Pseudophalacroma nasutum; l Metaphalacroma skogsbergii; m Citharistes regius. All to scale, bar = 10 μm
Mar Biodiv
Fig. 4 Light microscopic pictures of Phalacroma, all to the same scale of 10 μm. a P. porodictyum; b P. doryphorum; c P. sp.; d P. amandula; e P. rapa; f P. favus; g P. mitra; h P. capitulata; i P. cuneus; j P. argus; k P.
sp. 1; l P. hindmarchii; m P. operculoides; n P. parvulum; o P. apicata. All to scale, bar = 10 μm
Mar Biodiv
Fig. 5 Scanning electron microscopic pictures, all to the same scale of 10 μm. Thecal plates H2 and H3 (hypotheca plates 2 and 3), E2 and E3 (epitheca plates 2 and 3), the arrows show the sagittal suture. a
Phalacroma porodictyum; b P. doryphorum; c P. amandula; d cf. Latifascia sp.; e P. mitra; f P. rapa; g P. favus; h P. capitulata; i P. parvulum; j, k P. cf. contractum; l P. cuneus; m P. argus
genera Amphisolenia and Pseudophalacroma, and could not be identified yet. To the best of our knowledge, it is the first record of the genus Pseudophalacroma in this region. The closest offshore sampling station (st. 4540–4545, Fig. 1) to the CCZ sampling area within this study was about 850 km away (Kofoid and Skogsberg 1928). It seems that the area was poor in dinophysoid species, as only 14 were found
(Table 3; Kofoid and Skogsberg 1928). These species were concurrent with the species found in this study. Amphisolenia was represented by nine species within our samples (Tables 2 and 3). Six of these species were congruent with the species documented by Kofoid and Skogsberg (1928). Only two species, A. thrinax F.Schütt and A. bidentata, were found at stations closest to the CCZ area.
Mar Biodiv
Fig. 6 Scanning electron microscopic pictures a–g. All cells in overview ai–gi to the same scale of 100 μm, details of the apical and antapical cell parts aii–giii are to the scale of 10 μm. Light microscopic pictures h and i. a Amphisolenia sp. 1; b A. bidentata in lateral view; c A. bidentata in
dorso-lateral v iew; d A. sch auin sla ndii ; e A..palmata ; f A. palaeotheroides; g A. cf. palmata; h A. thrinax; i Triposolenia bicornis. All to scale, bar = 10 μm
Mar Biodiv
Fig. 7 Scanning electron micrographs of Ornithocercus species. a O. quadratus f. quadrata; b O. skogsbergii; c O. quadratus f. assimilis; d O. splendidus; e O. magnificus; f O. heteroporus; g O. steinii; h O. thumii. All to scale, bar = 50 μm
Mar Biodiv
Fig. 8 Scanning electron microscopic pictures of Parahistioneis and Histioneis. a Parahistioneis paraformis; b P. cf. para; c P. cf. pieltainii; d Histioneis cf. striata; e H. cf. crateriformis; f H. elongata; g H. alata; h H. biremis; i H. longicollis; j H. costata. All to scale, bar = 10 μm
Mar Biodiv Table 3 Dinophysoid genera with numbers of accepted planktonic species (worldwide) from Gómez (2012) in comparison with total species records of the present study, the closest sampled sites in the Pacific and eastern Pacific (Kofoid and Skogsberg 1928. ‘Not known’ genera were unknown at that time; ‘–’ not found within the samples
Genera
Gómez 2012 Accepted species
This study No. of found taxa
St. 4540-4545 (Kofoid and Skogsberg 1928) No. of found taxa
Eastern Pacific (Kofoid and Skogsberg 1928) No. of found taxa
Amphisolenia
37
9
2
26
Citharistes
2
1
―
2
Dinofurcula Dinophysis
2 78
― 15
― 3
2 20
Histioneis
52
8
―
24
Histiophysis Latifascia
1 2
― 1
― ―
1 2 (as Heteroschisma)
Metadinophysis Metaphalacroma
1 1
― 1
― ―
Not known Not known
Ornithocercus
15
9
5
9
Parahistioneis Phalacroma
13 69
3 16
― 4
7 31
Proheteroschisma Pseudophalacroma
1 1
― 2
― ―
Not known 0
Sinophysis Triposolenia
7 10 286
― 1 66
― ― 14
Not known 8 132
Specimens identified as A. cf. palmata showed differences in their antapical spine length and number (Fig. 6g). According to Kofoid and Skogsberg (1928), cells like the one shown (Fig. 6g) were identified as A. cf. palmata. F. von Stein’s first description and drawing of A. palmata showed longer spines (von Stein 1883), which have more similarities with the cell shown in Fig. 5e. Cells of Amphisolenia cf. lemmermanni were found at two stations (Table 2). The cell morphology showed the highest similarity with A. lemmermanni Kof., but the hypotheca was not as swollen as that described for the species (Kofoid 1907, pl. 14, figs. 88 and 89). Amphisolenia sp. 1 (Fig. 6a) was observed for the first time and showed a unique swelling at the antapical part at the right hypothecal plate. Further data are needed to verify whether it is a new species. Triposolenia was represented only by one specimen of T. bicornis in one sample (Table 2; Fig. 6i). The sample was taken with a vertical net tow from 150 m depth. Kofoid and Skogsberg (1928) reported eight species of the genus but none close to the CCZ (Table 3). Nevertheless, T. bicornis was reported from several sampling places from the southeastern and western Pacific and the coastline (Kofoid and Skogsberg 1928; Okolodkov and Gárate-Lizárraga 2006). The genus Dinophysis was well represented and found regularly within all samples, excluding most 80-μm net samples. Especially small species of Dinophysis could not be collected with large mesh sizes. The western CCZ sampling area seemed to be species-poor in general and Dinophysis was found rarely. The three species documented by Kofoid and
Skogsberg (1928), namely D. caudata Kent, D. exigua and D. hastata, and Dinophysis spp. recorded from the Mexican Pacific coast (Esqueda-Lara and Hernández-Becerril 2010), with the exception of D. uracanthoides Jørg., were also found within this study (Table 2). Dinophysis caudata was expected to be common (Kofoid and Skogsberg 1928), but only one cell was recorded in the ABYSSLINE A sample. The cell looked similar to the described young developmental stage (synonym: Dinophysis diegensis Kof.) of Dinophysis caudata (Okolodkov 2014, p. 25, pl. 2, fig. 8; Reguera and González-Gil 2001, p. 322, fig. 3 G and H) but was larger. The developmental stage was described as being about 55 μm in length (Reguera and González-Gil 2001). The observed cell was 70 μm in the present study. That corresponded to the size of D. acutissima (Gaarder 1954), but the prominent ‘pike’ of that species was missing. Dinophysis caudata was found close to the sampling site previously (Kofoid and Skogsberg 1928). Kofoid and Skogsberg (1928) described a high intra-specific morphological variation for D. fortii that includes the documented specimen (Fig. 2n). Dinophysis punctata cells were predominantly consistent with the original description (Jørgensen 1923). The identification of taxa within the D. hastata complex was difficult and the identity of two species, Dinophysis cf. phalacromoides and Dinophysis cf. uracanthoides, was uncertain. Both identifications are concurrent with morphological descriptions from Esqueda-Lara et al. (2013). Phalacroma is a widespread genus and was found regularly at all stations (Table 2). Offshore in the eastern Pacific, species
Mar Biodiv
seemed to be rare (Table 3; Kofoid and Skogsberg 1928). Only four species, namely P. argus F.Stein, P. cuneus F.Schütt, P. doryphorum and P. favus (Kof. & J.R.Michener) Abé were reported (Kofoid and Skogsberg 1928). About onethird of all the 47 Phalacroma species in the Pacific recorded by Kofoid and Skogsberg (1928) were found within this study (Table 2). One cell (Fig. 4m) was identified as P. cf. operculoides, because the morphology generally matched the original description and a later record (Schütt 1895; Haraguchi and Odebrecht 2010), but it had a more elongate hypotheca. A Phalacroma cf. rotundata cell seen in sample 10 was concurrent with the morphology of P. rotundata, but smaller. Cells documented as P. cf. parvulum (Fig. 5j, k) share the same morphology but were smaller than documented cells of P. parvulum (Jørgensen 1923; Kofoid and Skogsberg 1928; Schütt 1895). The discrimination between Phalacroma and Dinophysis followed the original descriptions (Kofoid and Skogsberg 1928; von Stein 1883). It was challenging for some taxa (e.g. P. rotundata), with no distinct features or character traits in between. The separation of Dinophysis and Phalacroma has been questioned (Tai and Skogsberg 1934) and Phalacroma has been synonymised with Dinophysis (Abé 1967a; Balech 1967). For that reason, only Dinophysis got recognised in some publications (Esqueda-Lara and Hernández-Becerril 2010; Nguyen et al. 2008). Based on molecular phylogenetic data, Phalacroma was reintroduced and epitypified (Jensen and Daugbjerg 2009). The separation of both genera received further support (Gómez et al. 2011; Handy et al. 2009; Jensen and Daugbjerg 2009) and is in general use again (Okolodkov 2014). As both genera seem to be polyphyletic (Gómez et al. 2011; Jensen and Daugbjerg 2009), further taxonomic revisions need to be done. The nine Ornithocercus species recorded (Table 2) were all known from the Pacific Ocean (Balech 1962; Esqueda-Lara and Hernández-Becerril 2010; Hernández Rosas et al. 2007; Kofoid and Skogsberg 1928; Omura et al. 2012) but only five in the open eastern Pacific (Table 3). The discrimination between Histioneis and Parahistioneis followed (Kofoid and Skogsberg 1928; von Stein 1883). Histioneis was characterised by the presence of a cross-rib on the postcingular list and a cingulum decidedly wider dorsally. Parahistioneis lacks a postcingular cross-rib and, usually, the precingular list was not stalked. The diversity and taxonomy was summarised by Gómez (2007). Five Histioneis species were identified to the species level (Table 2, Fig. 8), H. cf. costata had a posteriorly stronger elongated left sulcal list as described for the species and sometimes slight reticulations in the list edges (Fig. 8j), and Histioneis sp. was similar to H. cf. costata but had stronger ornamentation on the left sulcal list below the fission rib (Fig. 8j). Histioneis elongata Kof. & J.R.Michener, H. longicollis Kof. and H. biremis
F.Stein were the most frequently observed (Table 2). Two Parahistioneis species were identified (Table 2, Fig. 8a, b). Parahistioneis cf. pieltainii (Fig. 8c) was tentatively named as the taxonomy of the species is uncertain (Gómez 2007) and a cross-rib on the postcingular list indicated a possible classification in the genus Histioneis. This observation is in contrast to the original description (Osorio Tafall 1942). Of the 24 Histioneis and seven Parahistioneis species reported by Kofoid and Skogsberg (1928) from the eastern Pacific, none was documented by them offshore northwards of the equator (‘Albatross’ expedition, Fig. 1) nearby the investigated areas. Only two species are known for the genus Citharistes (Table 3) and one, C. regius F.Stein, was found regularly within the samples (Table 2). The species was recorded before in the Pacific Ocean, despite its scarcity (Omura et al. 2012). Metaphalacroma skogsbergii L.S.Tai was recorded in three samples (Table 2). It was originally described from Monterey Bay, California (Tai and Skogsberg 1934) and observed in the Pacific Ocean (Omura et al. 2012). The monospecific genus Pseudophalacroma has not been recorded offshore from the eastern Pacific yet, but has from the coastline of the Mexican Pacific (Okolodkov and GárateLizárraga 2006) and from the western Pacific (Omura et al. 2012). Pseudophalacroma nasutum (F.Stein) Jørg. occurred in several samples (Table 2). Within this study, a second morphotype was documented (Fig. 2q), which might be a new Pseudophalacroma species. Gómez et al. (2012) identified a species sampled in the Marmara Sea as Pseudophalacroma sp., but we are not convinced of the genus allocation. It could be a Metaphalacroma but further morphological data are needed for a reliable classification. For the genus Latifascia Loebl. & A.R.Loebl. (as Heteroschisma in Kofoid and Skogsberg 1928), two species are known (Gómez 2012). The genus Latifascia and its type, Latifascia inaequale (Kof. & Skogsb.) Loebl. & A.R.Loebl., was described from the eastern Pacific (Kofoid and Skogsberg 1928). The cell found in the CCZ (Fig. 5d) could not be unambiguously identified but was tentatively classified within the genus. It could be conspecific with the Latifascia cell documented from the Gulf of Mexico (Okolodkov 2014, pl. 3, fig. 5). The genus Dinofurcula Kof. & Skogsb., comprising only two species, was missing within our samples and was rarely documented previously in the south-eastern Pacific Ocean (Kofoid and Skogsberg 1928; Ochoa and Baylón 2005) and near the coast in the Mexican Pacific (Hernández-Becerril and Bravo-Sierra 2004). Comparing the different sampling techniques (20-μm net, 80-μm net, surface water only or vertical tow from 150 m depth to the surface, or pumped water from just below the surface filtered through a cascade collecting the 20–100-μm fraction), none was best for all dinophysoid taxa. Depending on the genus, different sampling techniques are preferable. Ornithocercus for example, with some relatively large and
Mar Biodiv
fragile species, were sampled most efficiently with the 20-μm horizontal net. Pumped and filtered seawater gave the worst results for the fragile cells. This was also true for Amphisolenia, with its large (long) and needle-shaped species. It is possible that some species of this genus were missed because of ineffective sampling with the large 80-μm net. Smaller and more spherical Dinophysis and Phalacroma species were best received in pumped and filtered samples. That method was simple, inexpensive and flexible. Additionally, it could be used not only for qualitative but also for quantitative analyses, if the filtered water volume would be measured during sampling. For obtaining the most diverse account, the different methods need to be applied in parallel (Table 2). In summary, the species diversity of dinophysoid dinoflagellates was unexpectedly high (66 taxa) and new morphotypes as well as new species have been found in the open ocean, in the CCZ, eastern Pacific. Although the amount of cells within the phytoplankton could not be quantified, it seems that dinophysoids were one of the dominating taxa within the dinoflagellate community and phytoplankton in general. Acknowledgements We thank the crews and teams of the MANGAN 2013 expedition, organised and financed by BGR (Bundesanstalt für Geowissenschaften und Rohstoffe), and of ABYSSLINE AB01, organised and financed by UK Seabed Resources, to which we acknowledge logistic and financial support, especially Lena Albers, Annika Janssen, Inga Mohrbeck and Pedro Martínez Arbizu, who collected phytoplankton samples during these cruises. We are in debt to Carsten Rühlemann (BGR) and Ralph Spickermann (UK Seabed Resources) for making the samples available to us and for their continuous support during the elaboration of this manuscript. We further thank two anonymous reviewers, who helped to improve our manuscript. Thanks to Janis Ortgies for the technical assistance.
References Abé TH (1967a) The armoured dinoflagellata: II. Prorocentridae and Dinophysidae (B). Dinophysis and its allied genera. Publ Seto Mar Biol Lab 15:37–78 Abé TH (1967b) The armoured dinoflagellata: II. Prorocentridae and Dinophysidae (C). Ornithocercus, Histioneis, Amphisolenia and others. Publ Seto Mar Biol Lab 15:79–116 Balech E (1962) Tintinnoinea y dinoflagellata del Pacífico: según material de las expediciones Norpac y Downwind del Instituto Scripps de Oceanografía. Imprenta y Casa Editora Coni, Buenos Aires Balech E (1967) Dinoflagelados nuevos o interesantes del Golfo de México y Caribe. Hidrobiologia 2:87–135 Couté A, Perrette C, Chomérat N (2012) Three Dinophyceae from Clipperton Island lagoon (eastern Pacific Ocean), including a description of Peridiniopsis cristata var. tubulifera var. nov. Bot Mar 55:59–71. doi:10.1515/bot-2011-121 Esqueda-Lara K, Hernández-Becerril DU (2010) Dinoflagelados microplanctónicos marinos del Pacífico central de México (Isla Isabel, Nayarit y costas de Jalisco y Colima). Instituto de Ciencias del Mar y Limnología. Universidad Nacional Autónoma de México, México
Esqueda-Lara K, Parra-Toriz D, Hernández-Becerril DU (2013) Morphology and taxonomy of Dinophysis species of the section Hastata (Dinoflagellata), including the description of Dinophysis conjuncta sp. nov., from the Mexican marine waters. J Mar Biol Assoc UK 93:1187–1202. doi:10.1017/S0025315412001750 Fensome RA, Taylor FJR, Norris G, Sarjeant WAS, Wharton DI, Williams GL (1993) A classification of living and fossil dinoflagellates. Micropaleontology Special Publication no. 7, American Museum of Natural History, New York Gaarder KR (1954) Dinoflagellate from the BMichael Sars^ North Atlantic Deep-Sea Expedition 1910. Rep Sci Res BMichael Sars^ North-Atl Deep-Sea Exped 2:1–62 Gómez F (2005) Histioneis (Dinophysiales, Dinophyceae) from the western Pacific Ocean. Bot Mar 48:421–425. doi:10.1515/bot.2005.055 Gómez F (2007) Synonymy and biogeography of the dinoflagellate genus Histioneis (Dinophysiales: Dinophyceae). Rev Biol Trop 55:459– 477 Gómez F (2012) A checklist and classification of living dinoflagellates (Dinoflagellata, Alveolata). Cicimar Oceanides 27:65–140 Gómez F, Claustre H, Souissi S (2008) Rarely reported dinoflagellates of the genera Ceratium, Gloeodinium, Histioneis, Oxytoxum and Prorocentrum (Dinophyceae) from the open southeast Pacific Ocean. Rev Biol Mar Oceanog 43:25–40 Gómez F, López-García P, Moreira D (2011) Molecular phylogeny of dinophysoid dinoflagellates: The systematic position of Oxyphysis oxytoxoides and the Dinophysis hastata group (Dinophysales, Dinophyceae). J Phycol 47:393–406. doi:10.1111/j.15298817.2011.00964 Gómez F, Moreira D, López-García P (2012) Sinophysis and Pseudophalacroma are distantly related to typical dinophysoid dinoflagellates (Dinophysales, Dinophyceae). J Eukaryot Microbiol 59:188–190. doi:10.1111/j.1550-7408.2011.00598 Hackett JD, Anderson DM, Erdner DL, Bhattacharya D (2004) Dinoflagellates: a remarkable evolutionary experiment. Am J Bot 91:1523–1534. doi:10.3732/ajb.91.10.1523 Handy SM, Bachvaroff TR, Timme RE, Coats DW, Kim S, Delwiche CF (2009) Phylogeny of four dinophysiacean genera (Dinophyceae, Dinophysiales) based on rDNA sequences from single cells and environmental samples. J Phycol 45:1163– 1174. doi:10.1111/j.1529-8817.2009.00738 Haraguchi L, Odebrecht C (2010) Dinophysiales (Dinophyceae) in the farthest Southern region of Brazil (Winter 2005, Summer 2007). Biota Neotropical 10:101–114. doi:10.1590/S1676-06032010000300011 Hernández-Becerril DU, Bravo-Sierra E (2004) Observations on a rare planktonic dinoflagellate, Dinofurcula cf. ultima (Dinophyceae), from the Mexican Pacific. Phycologia 43: 341–345. doi:10.2216/i0031-8884-43-4-341.1 Hernández Rosas A, Meave del Castillo ME, Zamudio-Resendiz ME, Castillo Rivera M (2007) Morphometry and distribution of species of the genus Ornithocercus (Dinophysiales: Dinophyta) from the Mexican Pacific. Hidrobiologica 17:257–272 Hernández-Becerril DU, Ceballos-Corona JGA, Esqueda-Lara K, Tovar-Salazar MA, León-Álvarez D (2008) Marine planktonic dinoflagellates of the order Dinophysiales (Dinophyta) from coasts of the tropical Mexican Pacific, including two new species of the genus Amphisolenia. J Mar Biol Assoc UK 88:1–15. doi:10.1017/S0025315408000143 Hoppenrath M (2000) Morphology and taxonomy of Sinophysis (Dinophyceae, Dinophysiales) including two new marine sanddwelling species from the North German Wadden Sea. Eur J Phycol 35:153–162. doi:10.1080/09670260010001735741 Hoppenrath M (2016) Dinoflagellate taxonomy—a review and proposal of a revised classification. Mar Biodiv. doi:10.1007/s12526-016-0471-8 Hoppenrath M, Chomérat N, Leander BS (2013) Molecular phylogeny of Sinophysis: evaluating the possible early evolutionary history of dinophysoid dinoflagellates. In: Lewis JM, Marret F, Bradley L
Mar Biodiv (eds) Biological and geological perspectives of dinoflagellates. The Micropalaeontological Society, Special Publications. Geological Society, London, pp 207–214 Jensen MH, Daugbjerg N (2009) Molecular phylogeny of selected species of the order Dinophysiales (Dinophyceae)—testing the hypothesis of a dinophysioid radiation. J Phycol 45:1136–1152 Jørgensen EH (1923) Mediterranean Dinophysiaceae. Report on the Danish oceanographical expeditions 1908–1910 to the Mediterranean and adjacent seas 2:1–48 Kofoid CA (1907) Reports on the Scientific results of the expedition to the eastern tropical pacific, in charge of Alexander Agassiz, by the U. S. Fish Commission Steamer BAlbatross,^ from October, 1904, to March, 1905, Lieutenant Commander L. M. Garrett, U. S. N., Commanding. IX. New species of dinoflagellates. Bull Mus Comp Zool 50:163–207 Kofoid CA, Michener JR (1911) New genera and species of dinoflagellates. Bull Mus Comp Zool Harvard Coll 54:267–302 Kofoid CA, Skogsberg T (1928) The dinoflagellata: the dinophysoidae. Vol 51 printed for the museum. Memoirs of the Museum of Comparative Zoology, Harvard University, Cambridge Le TT, Nguyen VN, Fukuyo Y (2012) Dinophysis (Dinophyceae) in Vietnamese waters. Coastal Mar Sci 35:73–77 Licea S, Zamudio ME, Luna R, Soto J (2004) Free-living dinoflagellates in the southern Gulf of Mexico: Report of data (1979–2002). Phycol Res 52:419–428 Marshall HG (1976) Phytoplankton distribution along the eastern coast of the USA. I. Phytoplankton composition. Mar Biol 38:81–89 Nguyen VN, Omura T, Furuya K, Fukuyo Y (2008) Dinophysis (Dinophyceae) in the pelagic waters of central and western Pacific. La Mer 46:29–36 Ochoa N, Baylón M (2005) Dinofurcula cf. ventralis in the central coast of Peru and the first report of two Protoperidinium species. Rev Peru Biol 12:377–382 Ojeda A (1999) Contribution to the knowledge on dinoflagellates (Dinophyceae) of the order Dinophysiales in the Canary Islands waters. Bol Mus Munic Funchal 51:53–84
Okolodkov YB (2014) Dinophysiales (Dinophyceae) of the National Park Sistema Arrecifal Veracruzano, Gulf of Mexico, with a key for identification. Acta Bot Mex 106:9–71 Okolodkov YB, Gárate-Lizárraga I (2006) An annotated checklist of dinoflagellates (Dinophyceae) from the Mexican Pacific. Acta Botanica Mexicana 1–154 Omura T, Iwataki M, Borja VM, Takayama H, Fukuyo Y (2012) Marine phytoplankton of the Western Pacific. Kouseisha Kou-seikaku, Tokyo Osorio Tafall, BF (1942) Notas sobre algunos dinoflagelados fitoplanctónicos marinos de México con descripción de nuevas especies. A. Esc Nal de Cienc Biol 2:435–450 Parra-Toriz D, Hernández-Becerril DU, Esqueda-Lara K (2014) Phalacroma gibbosum sp. nov. (Dinophyceae) from the southern Gulf of Mexico. Nova Hedwigia 99:83–96 Reguera B, González-Gil S (2001) Small cell and intermediate cell formation in species of Dinophysis (Dinophyceae, Dinophysiales). J Phycol 37:318–333 Schiller J (1933) Dinoflagellatae (Peridineae). In: Rabenhorst L (ed) Kryptogamen-Flora von Deutschland, Österreich und der Schweiz, vol 10 part 1, 2nd edn. Akademische Verlagsgesellschaft, Leipzig Schütt F (1895) Die Peridineen der Plankton-Expedition. I. Theil. Studien über die Zellen der Peridineen. Lipsius & Tischler, Kiel Silva PC (1994) Report of the Committee for Algae: 2. Taxon 43:257– 264. doi:10.2307/1222885 Steidinger KA, Faust MA, Hernández-Becerril DU (2009) Dinoflagellates (Dinoflagellata) of the Gulf of Mexico. In: Felder DL, Camp DK (eds) Gulf of Mexico origin, waters, and biota. Texas A&M University Press, College Station, TX, vol 1, pp 131–154 Tai L-S, Skogsberg TAGE (1934) Studies on the Dinophysoidae, marine armored dinoflagellates, of Monterey Bay, California. Archiv Protistenkd 82:380–482 Taylor FJR, Hoppenrath M, Saldarriaga JF (2008) Dinoflagellate diversity and distribution. Biodivers Conserv 17:407–418. doi:10.1007/s10531-007-9258-3 von Stein FR (1883) Der Organismus der Infusionsthiere nach eigenen Forschungen in systematischer Reihenfolge bearbeitet. Engelmann, Leipzig