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Protoperidinium (DINOPHYCEAE) SPECIES IN THE GULF OF
CALIFORNIA AND OFF THE COAST OF BAJA CALIFORNIA
Trabajo recibido el 4 de
abril de 1991 y aceptado para su publicación el 9 de julio de
1991.
David U. Hernández-Becerril
Centro de Investigaciones de Quintana Roo (CIQRO),
Depto. de Ecología Acuática, Apartado postal 424, Chetumal, Q.R.
77000 MÉXICO.
El análisis de muestras de plancton colectadas
con red en el Golfo de California y costas de Baja California, ha permitido la
identificación de 34 especies y una variedad del dinoflagelado
género Protoperidinium Bergh. Se citan seis especies
por primera vez para aguas mexicanas y 13 son nuevos registros para el Golfo de
California. Los grupos de especies no son netamente tropicales, sino que se
componen de especies cosmopolitas, templadas y subtropicales, habiendo pocas
típicamente tropicales. La mayoría de las especies se ilustran
por medio de microscopía de luz y electrónica de barrido. Se
proponen dos nuevos cambios taxonómicos: Protoperidinium
robustum (Meunier) nov. comb. y P.
murrayi (Kofoid) nov. comb.
Net plankton samples from the Gulf of California and
off the coasts of Baja California were analyzed and thirty-four species and one
variety of the dinoflagellate genus Protoperidinium Bergh
are reported here. Six species are cited for the first time in Mexican waters
and thirteen species are new records in the Gulf of California. The groups of
species found are not completely tropical, as few species are truly tropical in
distribution, but there are many cosmopolitan, temperate, subtropical species.
Most of the species are illustrated by light and scanning electron microscopy.
Two new taxonomic changes are proposed: Protoperidinium
robustum (Meunier) nov. comb. and P.
murrayi (Kofoid) nov. comb.
The armoured dinoflagellate genus Protoperidinium Bergh is one of the most important genera in marine phytoplankton, as it is widely distributed around the world and contains a large number of species. This genus has been largely studied by Balech (1949, 1951, 1964, 1973, 1974, 1976) who found that there are basic differences between Protoperidinium and a very closely related genus, Peridinium Ehrenberg. Positive identification to species level is not always easy, and identification is based in the cell size and shape, the plates arrangernent, the position of the cingulum, the structure of the sulcus and the presence of apical or antapical spines, horns or ribs. Several recent studies have used Scanning Electron Microscopy (SEM) to observe detafis of the plates, apical pores, sulcus, or amentation of the theca, etc. (Gocht & Netzel, 1974: Ricard, 1974; Balech, 1975; Taylor, 1976; Dodge, 1983. 1987; Economou-Amilli, 1986). In waters from the Gulf of California and off the coasts of Baja-California, many Protoperidinium species have been reported (e.g. Klement, 1964; Round, 1967) and for the Gulf of California alone 34 taxa have been listed (Hernández-Becerril, 1987). Some species have not been recorded under their present taxonomic status, and other small species have been overlooked. It is the purpose of this paper to give an illustrated guide lo the genus in the arcas mentioned above. STUDY AREAThe Gulf of Califomia is located between 25-32° N and 107-115° W, in the Eastern Pacific Ocean (Fig. I). The weather is rather continental than oceanic, and according to its hydrology the Gulf has been divided into four parts. The central part with strong mixture and turbulence supports high phytoplankton populations, especially dominated by diatoms, while the southern part is less rich in nutrients and with a complex termohaline structure, showing a planktonica flora characteristic of warm waters. The coastal area of Baja California, in the Pacific Ocean, is constantly affected by the California current and by upwellings occurring in winter. The Davidson's countercurrent contributes warm water to the area and also carries tropical forms, its intensity depending on the season of the year. Both regions are different: the Gulf of Califomia may be considered as a diverse and rich, semi-open system, while the area of Baja California coasts is a more open, changing system, where mixed populations are found. MATERIAL AND METHODSNet material from five cruises have been analyzed. Three cruises were made in the Gulf of California in November-December, 1984, in March, 1985 and in July, 1986, and two cruises along coasts of Baja California in August, 1985 and in June, 1986. Fig. 1 shows the stations where Protoperidinium species were found. For details of sampling see Hernández-Becerril (1988). Observations of Protoperidinium species were made using a light microscope (LM) Olympus CH, phase contrast and bright field. Rinsed and critica-point dried material was used for the scanning electron microscopy (SEM) Phillips 501. In most cases, single cells were isolated with a micropippete and put onto coverslips, airdried, and then coated with gold for SEM study.  Figure 1. Location of sampling stations where Protoperidinium species were found in the Gulf of California and off the coast of Baja California. RESULTS AND DISCUSSIONThirty-four species and one variety were encountered in the samples. Systematic arrangement follows Balech (1984) and Dodge (1982); relevant literature for identification is included for each species and conspicuous synonyms are given. The measurements are given in um, indicating 1= total length, w= total or maximum width. Information about general distribution of species was gathered from several references. Genus Protoperidinium Bergh Subgenus Archaeperidinium Jörgensen Protoperidinium avellana ? (Meunier) Balech Fig. 21. Balech, 1974, p. -54; Dodge, 1982, p. 173, fig. 19 F-H. =Peridinium avellana (Meunier) Lebour Lebour, 1925, p. 108. pl. 17, fig. 1. =Properidinium avellana Meunier Meunier, 1919, p. 56, p1. 18, figs. 32-41. Brackis and marine species, temperate ? Sta. 7. One single, little collapsed specimen observed. Measurements: 48 um 1, 45 um w. Protoperidinium excentricum (Paulsen) Balech Figs. 16, 17. Balech, 1974, p. 54; Dodge, 1982, p. 174, fig. 19 J, K. =Peridinium excentricum Paulsen Paulsen, 1907, p. 14, fig. 17. Temperate to subtropical, neritic. Sta. A, C, F. Measurements: 35-38 um 1, 75-86 um w. Protoperidinium minutum (Kofoid) Loeblich Fig. 19. Dodge, 1982, p. 174, fig. 19 C, D, pl. 4 b, c =Peridinium minutum Kofoid Kofoid, 1907a, p. 310, pl. 31, figs. 42-45. Subtropical to temperate, neritic: ? Sta. R9. Measurements: 43-45 um 1, 38-39 um w. New record for the Gulf of California.. Protoperidinium robustum (Meunier) Hernández-Becerril nov. comb. Figs. 1, 18. Basyonym - Peridinium robustum Meunier, 1910, p. 41, pl. 41, figs. 33-37. This could be a temperate to cold-water species. Sta. R7. Measurements: 60-68 um 1, 53-60 um w. New record for mexican waters and the Gulf of California. Only two previous records of this species (Meunier, 1910; Lebour, 1925) make its distribution unknown. Protoperidinium thorianum (Paulsen) Balech Balech, 1973, p. 347, p1. 1, figs. 1-8; Dodge, 1982, p. 176. fig. 19E. =Peridinium thorianum Paulsen Paulsen, 1908, p. 62, fig. 81. =Properidinium thorianum (Paulsen) Meunier Meunier, 1919, p. 57, p1. 18, figs. 42-46. Temperate to warm-water in distribution. Sta. R9. Measurements: 58-65 um 1, 56-63 um w. New record in the Gulf of California. Subgenus Protoperidinium (Gran) Balech Group Orthoperidinium Section Oceanica Jórgensen Protoperidinium caludicans (Paulsen) Balech Figs. 7, 20. Balech, 1974, p. 57; Dodge, 1982, p. 182, fig. 20 G, H. =Peridinium claudicans Paulsen Paulsen, 1907, p. 16, fig. 22. Cosmopolitan, neritic species. Sta. 7, F, I, R5, R7, R8. Measurements: 85-107 um 1, 75-78 um w. Protoperidinium depressum (Baley) Balech Fig. 22. Balech, 1974, p. 57; Dodge, 1982, p. 177, fig. 20 A, pl. 5 e = Peridinium depressum Bailey Bailey, 1854, p. 12, figs. 33, 34. Cosmopolitan, oceanic c and neritic. Sta. 1, 4, 7, 9, 10, 15,38,39, B, F, R6, R7, R9. Measurements: 138-145 um 1, 127-135 um w. Protoperidinium murrayi (Kofoid) Hernández-Becerril nov. comb. Figs. 6, 27. Basyonym= Peridinium murrayi Kofoid, 1907b, p. 176, p1. 5, fig. 29. Synonym= Peridinium murrayi var. occidentalis Pavillard, 1930, p. 8, fig. 9 B. Synonym= Peridinium murrayi var. orientalis Matzenauer, 1933, p. 465, fig. 46 b. Tropical and subtropical species. Sta. C, F. Measurements: 190-208 um 1, 118-125 um w. P. murrayi is a very common species within the Gulf of California (Hernández-Becerril, 1987). Balech (1974) did not transfer this species into Protoperidinium, but blaced Peridinium oblongum Aurivillius as a synonym of P. oceanicum with no mention of P. murrayi. The larger size, body shape (not as depressed as P. oceanicum), and the more developed apical and antiapical horns in P. murrayi are characteristics to separate it from P. oceanicum. Léger (1973) discussed the validation of P. murrayi and suggested it could be a variety of P. oceanicum, and recently Balech (1988) mentioned it as a form of warm and oceanic waters. Therefore, further studies on the fine morphology and ultrastructure are still necessary. Protoperidinium oceanicum (Vanhöffen) Balech Balech, 1974, p. 57; Dodge, 1982, p. 180, fig. 20 E. =Peridinium ocenicum Vanhöffen Paulsen, 1908, p. 54, fig. 69. Cosmopolitan, oceanic. Sta. 1, 7, 10, 15, 38, B, E, R6. Measurements: 112-118 um 1, 80-88 um w. See remarks for P. Murrayi. Protoperidinium venustum (Matzenauer) Balech Fig. 23. Balech, 1974, p. 57; Balech, 1988, p. 86, pl. 24, figs. 1-4. =Peridinium venustum Matzenauer Matzenauer, 1933, p. 464, fig. 45. Warm-water species. Sta. 2, 3, 18, R8. Measurements: 114-120 um 1, 85-97 um w. It could be recorded as P. oceanicum earlier in the Gulf of California, as it is a new record for this area. The relationship between this species and P. oblongum (Aurivillius) Parke et Dodge is not clear, and they may be synonymous. Section Tabulata Jörgensen Protoperidinium punctulatum (Paulsen) Balech Figs. 3. 25. 28. Balech, 1974, 58; Dodge, 1982, p. 183, fig. 20 L, M. =Peridinium punclualatum Paulsen Paulsen, 1907, p. 19 fig. 28. =Peridinium subinerme var. punctulatum (Paulsen) Schiller Schiller, 1937, p. 245, fig. 245 a, b. Oceanic and neritic. Sta. F. Measurements: 58-64 um 1, 66-71 um w. New record for the Gulf of California. Section Conica Jörgensen Protoperidinium biconicum (Dangeard) Balech Balech, 1974, p. 58. =Peridinium biconicum Dangeard Schiller, 1937, p. 230, fig. 227 a-e. Temperate and subtropical. Sta. F. Measurements: 82 um 1, 62 um w. Just one specimen found. Protoperidinium conicum (Gran) Balech Figs. 5, 24. Balech, 1974, p. 58; Dodge, 1982, p. fig. 21 G, H. =Peridinium conicum (Gran) Ostenfelt et Schmidt Paulsen, 1908, p. 58, fig. 74. Cosmopolitan. Sta. 38, F, R5, R6, R7, R9. Measurements: 86-120 um 1, 90-121 um w. Protoperidinium latissimum (Kofoid) Balech Fig. 2, 3 1. Balech, 1974, p. 67. =Peridinium latissimum Kofoid Kofoid, 1907b, p. 175, figs. 31, 32. =Peridinium pentagonum var. latissimum (Kofoid) Schiller Schiller, 1937, p. 242, fig. 243. =Protoperidinium exiquipes (Mangin) Dodge Dodge, 1985, p. 54. Warm-water species. Sta. C, F, R5. Measurements: 75-89 um 1, 93-99 um w. Considered by Balech (1974) as a Para-peridinoid species, i.e. plate 1' hexagonal, but here it appeared as a Ortho-peridinoid species. This species could have both types of tabulation (Balech, 1988). Protoperidinium obtusum (Karsten) Parke et Dodge Figs. 4, 26. Parke & Dodge, 1976, p. 545. =Peridinium obtusum Karsten Lebour, 1925, p. 121, p1. 24, figs. 2a.2d. Temperate, tropical and subtropical. Sta. 10, F, R6, R7. Measurements: 88-90 um 1, 81-85 um w. Species possibily misidentified with P. Leonis (Pav.) Balech earlier in the Gulf of California and it is a new record for this area. Protoperidinium pentagonum (Gran) Balech Balech, 1974, p. 59; Dodge, 1982, p. 188, fig. 21 L-N. =Peridinium pentagonum Gran Paulsen, 1908, p. 59, fig. 76. Temperate to subtropical, neritic. Sta. A, F, J, R5. Measurements: 62-69 um 1, 78-82 um w. Peridinium subinerme (Paulsen) Loeblich Balech, 1974, p. 60, fig. 78 a, f, non a-d. Temperate to subtropical. Sta. A, I. Measurements: 52-60 um l, 68-75 um w. Group Metaperidinum Section Piriformia Jórgensen Protoperidinium latispinum (Mangin) Balech Fig. 30. Balech, 1974, p. 62. =Peridinium latispinum Mangin Schiller, 1973, p. 193, fig. 190 A a-d. Warm-water species. Sta. 2, 3, 7, 38, I. Measurements: 72-74 um 1, 40-42 um w. New record for Mexican waters and the Gulf of California. Protoperidinium mediterraneum (Kofoid) Balech Figs. 32, 33. Balech, 1974, p. 62. =Peridinium steinii var. mediterraneum Kofoid Kofoid, 1909, p. 40, fígs. 1-11 =Peridinium mediterraneum (Kofoid) Balech Balech, 1964, p. 184, p1. 2, figs. 26-35. =Peridinium longicollum Pavillard Taylor, 1976, p. 156, p1. 32, fig. 346. Warm-water species. Sta. 1, 7, 1. Measurements: 85-95 um 1, 55-61 um w. New record for the Gulf of California. Protoperidinium ovirme (Dangeard) Balech fo Figs. 8, 9. Balech, 1974, p. 63; Balech, 1988, p. 96, p1. 33, fígs. 5-8. Warm-water species. Sta. R8. Measurements: 66-69 um 1, 41-46 um w. New record in Mexican waters and in the Gulf of California. Protoperidinium aff. pariventer Balech Fig. 40. Balech, 1988, p. 105, p1. 39, figs. 10-14. Warm-water to temperate species. Sta. A, F. Measurements: 61-71 um 1, 57-67 um w. Protoperidinium pyrifornie var. breve (Paulsen) Balech Figs. 14,37. Balech, 1988, p. 94, p1. 31, figs. 20-21. =Peridinium breve Paulsen Paulsen, 1907, p. 13. Apparently this is a cold-water species. Sta. 10. Measurements: 48-52 um 1, 42-46 um w. Protoperidinium pyrum (Balech) Balech Balech, 1974, p. 63; Balech, 1988, p. 94, p1. 31, fig. 22, pl. 32, fígs. 1-4. Cold-water but tolerant species. Sta. 7. Measurements: 92-95 um 1, 65-67 um w. New record for Mexican waters. Protoperidinium quarnerense (Schöder) Balech Fig. 44. Balech, 1974, p. 61; Balech, 1976, p. 33, fig. 3. =Peridinium globulus var. quarnerense Schöder Schiller, 1937, p. 184, fig. 186. Tropical and subtropical. Sta. C, E. Measurements: 53 um 1, 43 um w. Protoperidiniuni simulum (Paulsen) Balech Fig. 45. Balech, 1974, p. 61; Balech, 1988, p. 112, p1. 45, figs. 2-5. =Peridinium simulum Paulsen Halim, 1960, pl. 2, fig. 28. Temperate to subtropical. Sta. R9. Measurements: 63 um 1, 75 um w. This is a new record for Mexican waters and the Gulf of California. Protoperidiniuni steinii? (Jorgensen) Balech Fig. 42. Balech, 1974, p. 63; Pesantes, 1978, p. 40, p1. 22, figs. 6, 7. =Peridinium steinii Jörgensen Paulsen, 1908, p. 47, fig. 58. Temperate to subtropical, oceanic and neritic. Sta. 1, A, F. Measurements: 78-84 um 1, 45-55 um w. Section Divergentia Jörgensen Protoperidiniuni brochii (Kofoid et Swezy) Balech Balech, 1974, p. 60; Pesantes., 1978, p. 31, p1. 19, figs. 5 -11. =Peridinium brochi Kofoid et Swezy Kofoid & Swezy, 192 1, o. 183. =Peridinium adriaticum Broch non Schmarda Broch, 1910, p. 19 1, fig. 8. Temperate to subtropical. Sta. 10, 15, F, J. Measurements: 73.90 um 1, 60-69 um w. Protoperidinium crassipes (Kofoid) Balech Figs. 35, 36. Balech, 1974, p. 60; Pesantes, 1978, p. 32, p. 20, fígs. 1-3. =Peridinium crassipes Kofoid Broch, 1910, p. 193, fig. 9 Subtropical, neritic. Sta. 1, 3, 8-10, A. Measurements: 65-68 um 1, 70-78 um w There is discussion if P. curtipes (Jörgensen) Balech is, a synonym of P. crassipes; according to some authors (Elibrächer, 1975; Dodge, 1982) the differences are basically the color of the cell content, body shape, sulcal plates and the apical horn, which is more prominent in P. curtipes. Protoperidiniuni divergens (Ehrenberg) Balech Figs. 13, 29. Balech, 1974, p. 60; Economou-Amilli, 1986, p. 356. fígs. 20-31. =Peridinium divergens Ehrenberg Paulsen, 1908, p. 56, fig. 72. Temperate, oceanic. Sta. 7, 9, 10, 14. Measurements: 112-145 um 1, 103-115 um w. Protoperidinium elegans (Cleve) Balech Figs. 12, 39. Balech, 1974, p. 66; Pesantes, 1978, p. 33, p1. 22, fígs. 1, 2. =Peridinium elegans Cleve Cleve, 1900, p. 16, figs. 15, 16. Tropical and subtropical. Sta. A, I. Measurements: 166-175 um 1, 131-142 um w. One specime was found having a smaller size (100 um 1, 70 um w), which could be regarded as a "dwarf" from of this species. Protoperidinium grande (Kofoid) Balech Fig. 11. Balech, 1974, p. 60; Pesantes, 1978, p. 34, pl. 23, figs. 9-11. =Peridinium grande Kofoid Kofoid, 1907b, p. 174, p1. 5, fig. 28. Tropical and subtropical. Sta. 15, I Measurements: 173-190 um 1, 104-126 um w. New record for the Gulf of California. Dodge's (1985) figure of this species apparently shows P. elegans. Group Paraperidinium Section Pellucida Jórgensen Protoperidinium longipes (Karsten) Balech Figs. 15, 41. Balech, 1974, p. 67; Pesantes, 1978, p. 35, pl. 23, fígs. 5, 6. =Peridinium longipes Karsten Karsten, 1907, p. 418, pl. 53, fig. 6 a, b. =Peridinium duabolus var. longipes (Karsten) Taylor Taulor, 1976, p. 162, pí. 32, fig. 354. Tropical and subtropical. Sta. A, I. Measurements: 120-123 um 1, 47-59 um w. Schiller (1937) placed Peridinium longipes as a synonym of P. diabolus Cleve, and later Tylor (1976) proposed P. longipes as a varitey of P. diabolus; Balech (1974) has separeted them. The specimens found here were identified as P. longipes after comparision with the modern description of P. diabolus (Balech, 1976). In P. longipes the apical horn is finer, more elongated, the epitheca is nearly tringular and the antapical spines are relatively longer and more divergent than P. diabolus. The reticulation pattern is also different in both species. Couté and Iltis' (1985) figure of P. diabolus could really show P. longipes. Abé (1981) stated Peridinium globosum (Gourret) Abé as the name that has priority over P. longipes. Protoperidinium pellucidum Bergh Fig. 43. Bergh, 1881, p. 227, p1, 15, figs. 46-48; Dodge, 1982, p. 202, fig. 23 J, K, pl. 5c. =Peridinium pellucidum (Bergh) Schütt Paulsen, 1908, p. 49, fig. 61. Temperate, neritic and oceanic. Sta. 14, I. Measurements: 45-53 um 1, 41-55 um w. The hipothecal pore (Dodge, 1987) is clearly seen in this species. Protoperidinium tenussimum (Kofoid) Balech Figs. 10, 38. Balech, 1974, p. 67; Sournia et al., 1979, p. 196, fig. 45. =Peridinium tenuissimum Kofoid Kofoid, 1907b, p. 176, pl. 5, fig. 34. =Peridinium crassiformis Abé Abé, 1981, p. 240, fig. 27 (176-179). Temperate to tropical, oceanic ? Sta. C, F. Measurements: 64-75 um 1, 30-35 um w. New record for the Gulf of California. Protoperidinium tristyIum (Stein) Balech Fig. 34. Balech, 1974, p. 67; Economou-Amilli, 1986, p. 356, figs. 14-19. =Peridinium tristylum Stein Stein, 1883, pl. 9, figs. 15-17. Temperate and warm-water species. Sta. F. Measurements: 7581 um 1, 56-58 um w. New record for Mexican waters and the Gulf of California. ConclusionesFrom the material collected, twenty-seven samples contained at least one Protoperidinium species: 15 samples in the Gulf of California and 12 from coasts of Baja Califomia. In the Gulf a larger number of species than in Baja California coasts was detected (31 and 17 respectively). Thirty-four species and one variety were found. Six species are cited for the first time in Mexican waters: Protoperidinium latispinum, P. oviforme, P. pyrum, P. robustum, P. simulum and P. tristylum. For the Gulf of California, thirteen are indicated to be new records: all cited above, except P. pyrum, plus P. grande, P. mediterraneum, P. minutun, P. obtusum, P. punctualtum, P. tenuissimun, P. thorianum and P. venustum. Two new combinations are proposed here: Protoperidinium robustum, a species thought to be cold-water in distribution, and P. murrayi, a rather common tropical and subtropical species, closely related to P. oceanicum. AgradecimientosI thank and appreciate correspondence and advice by profs. E. Balech, J..D. Dodge, and A. Souriana about identification and comments on taxonomy. Dr. DJ. Peterson reviewed critically one of the preliminary manuscripts. 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 Plate 1. (CON). 1. Protoperidinium robustum. 2. P. latissimum. 3. P. puntulatum. 4. P. obtusum. S. P. conicum. 6. P. murrayi. 7. P. claudicans. 8, 9. P. oviforme. 10. P. tenuissinum. 11. P. grande. 12. P. elegans. Scale bars = 50 um, Figs. 6,11,12, = 20 um, Figs. 1-5, 7-10.  Plate 2. Figs. 13-15 (CON). 16-24 (SEM). 13. Protoperidinium divergens. 14. P. pyriforme var. breve 15. P. longipes. 16, 17. P. excentricum, antapical and apical views, respectively. 18. P. robustum. 19. P. minutum. 20. P. claudicans. 21. P. avellana ?. 22. P. depressum. 23. P. venustum. 24. P. conicum. Scale bars = 50 um, 23. P. venustum. 24. P. conicuUV@"bars = 50 un; Fig. 13, = 20 un; Figs. 14-18, 10.  Plate 3. Fig. 25-36 (SEM) 25, 28. Protoperidinium puntulatum, ventral and dorsal views. 26. P. obtusum. 27. P. murrayi. 29. P. divergeens. 30. P. latispinum. 31. P. latissimum. 32, 33. P. mediterraneum, ventral and apical views, respectively. 34. P. trisiylum. 35,36. P. crassipes, two different cells in ventral view. Scale bars = 20 um, Figs. 26, 27, 29, 3 1, = 10 um, Figs. 25, 28, 30, 32-36.  Plate 4. Figs. 37-45 (SEM). 37. Protoperidinium pyriforme var. breve. 38. P. tenuissimum. 39. P. elegans. 40. P. aff. parviventer. 4 1. P. longipes. 42. P. steinii ?. 43. P. pellucidum 44. P. quernerense. 45. P. simulum. Scale bars = 20 obtusum. Figs. 39,41, = 10 um, Figs-37,38,40,42-45. An. Inst. Cienc. del Mar y Limnol. Univ. Nal. Autón. México, 18(1): 89-98 (1991)
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