On the taxonomy of the family Podolampadaceae Lindemann (Dinophyceae) with descriptions of three new genera

ELSEVIER

Review of Palaeobotany and Palynology 84 (1994) 73 99

REVIEW OF PALAEOBOTANY AND PALYNOLOGY

On the taxonomy of the family Podolampadaceae Lindemann (Dinophyceae) with descriptions of three new genera M.C. Carbonell-Moore Oregon State University, College of Oceanic and Atmospheric Sciences, Oceanography Admin. Bldg. 104, Corvallis, OR 97331, USA Received 24 April 1993; revised and accepted 19 April 1994

Abstract

Dinoflagellate cells from the family Podolampadaceae from multiple locations in the world's oceans, were studied under the scanning electron microscope. The plate formula of the family is redefined based upon plate homology comparisons between the hypotheca of the closely related Peridinioid genus Diplopsalis Bergh and the hypotheca of different Podolampadacean genera. As in Diplopsalis, five postcingular plates and only one antapical plate are found in the hypotheca of the Podolampadaceans. The Podolampadacean plate formula may be written as: Po Pt X 3' la 5" 3C 4-5S 4 - 5 " 1"', where Pt refers to the cover plate in the apical pore complex (APC). Three new genera (Mysticella, Gaarderia and Heterobractum) are proposed on the basis of the apical pore types, cell compression and/or cell bilateral asymmetry. A new combination for the former Blepharocysta striata Schtitt is proposed as Mysticella striata (Schiitt) Carbonell-Moore, comb. nov. Three types of APC were found in the Podolampadaceans: Type 1: Pore plate with ridges and pores; cover plate with only a small protuberance; this apical pore is typical of Blepharocysta. Type 2: Pores but no ridges on the pore plate; cover plate with a small spine. Lissodinium Matzenauer, emend. Carbonell-Moore and Mysticella Carbonell-Moore, gen. nov. illustrate this type of apical pore. Type 3: Pore plate as in Type 2. Cover and canal plate with a continuous pronounced ridge. Gaarderia CarbonellMoore, gen. nov. and Heterobractum Carbonell-Moore, gen. nov. represent this kind of apical pore. A broad range in cell bilateral asymmetry and cell compression resulting in a pronounced cell distortion was evident in these dinoflagellates. In Blepharocysta there is almost no cell compression, while most species of Podolampas are dorso-ventrally compressed. Cells of Mysticella species may present no compression or may be slightly dorso-ventrally compressed. Lissodinium is laterally compressed and shows the highest degree of bilateral symmetry within the family. A unique bilateral plate asymmetry (and no cell compression) is observed in Heterobractum Carbonell-Moore, gen. nov. A pronounced cell distortion is found in the different species of Gaarderia Carbonell-Moore, gen. nov. Of all plate series, the cingular series show the most variation in both development (narrow to very wide) and relative plate size within the same series. Zygotic forms as evidence of a sexual life cycle were observed in some species. An evolutionary trend is briefly discussed.

0034-6667/94/$7.00 © 1994 Elsevier Science B.V. All rights reserved SSDI 0034-6667 (94)00069-V

74

M. C~ Carbonell-Moore/Review ol Palaeobotany aml Pa@nology 84 i 1994) 73 99

I. Introduction

The dinoflagellates included in the family Podolampadaceae lack both a depressed cingulum and sulcus. Three genera have been described within this family: Blepharoo,sta (Ehrenberg) Stein, Podolarnpas Stein, and Lissodinium Matzenauer. Blepharoo'stacells are spherical without spines, Podolampas cells are pyriform and show strong antapical spines while pebble-like laterally compressed cells are included in Lissodinium. Some species of Lissodinium may present a small antapical spine (Carbonell-Moore, 1993). The Podolampadaceans were first associated with the Peridinioids by Btitschli (1885). Two authors, Schatt (1895) and Balech (1954, 1963, 1988) have compared the three large plates which occupy the lowermost half of the cell to the cingular plates of most Peridinioids. Most authors who have studied these dinoflagellates have considered the lack of delimitations of a cingulum by either lists or by a depression as if the cingulum were absent altogether and have provided many different plate formulas which are summarized in Table 1. Among these authors, Kofoid (1909) in a study of Podolampas elegans SchOtt was the first to present a plate tabulation formula for the Podolampadaceans. His formula was 2' la 6" 3" 4"". He believed that even though the flagella were located in a homologous place as in other Peridinioids, there were no structural features that could enable the flagella to be held in place in

such an exposed position. Nie ( 1939, 1942) studied Blepharocysta splendor-maris (Ehrenberg) Stein, Podolampas bipes Stein, and P. palmipes Stein. He modified the formula to Y l a 5" 4S 3'" 4 5"", and differentiated for the first time the four sulcal plates as a different plate series. He related these plates to the homologous plate series in Protoperidinium Bergh. However, one of his "sulcal" plates belonged to a different plate series. This left 1 2 sulcal plates to be later identified by Balech (1963). Rampi (1941) presented two plate formulas, two for Blepharocysta and one for Podolampas. Ignoring Nie's earlier works, Gaarder (1954) provided a new interpretation of Kofoid's (1909) studies on thecal plates of Podolampas elegans. She found the same number of plates but in disagreement with Kofoid, she identified three apical plates instead of two. Nie had also found three apical plates. In the hypotheca, Gaarder identified the presence of two intercalary and four antapical plates. Her formula may be written as 3' la 5" 4"' 2p 4"". Nevertheless, she recognized that this formula could not be fully applied to Blepharoo'sta and Podolampas. Ab6 (1966) followed Nie's (1942) approach of relating the Podolampadaceans to the Peridinioids and used Diplopsalis sensu Dodge and Toriumi (1993) under the name Diplopsalopsis in his study of the family Podolampadaceae. He also concluded the absence of a cingulum based upon the fact that he found pores along the lower suture of the precingular plates which were analogous to pores

Table I Plate tabulation formulas for the family Podolampadaceae discussed in this paper Author

Plate tabulation formulas

Kofoid (1909) Nie (1939, 1942) Rampi ( 1941 )~ Rampi (1941) u Gaarder ( 19541 Balech (1963) Abe (1966) Carbonell-Moore ( 1991 )c This study

2' 3' 2' 1' 2' 3' 3' 3' 3' 3'

~For Podolampas. hFor Blepharocysta, ~For Lissodinium.

APC (Po, X) A PC (Po, Pt, X I

la la la 0 2a la la Ia la la

6" 5" 6" 5" 6" 5" 5" 5" 5" 5"

4S

3'" 3"' 3'"

4"" 4 5"" 4"': 3"':

3 6'" 2p 3C 3C 3C

4 5S 4S 5S 4 5S

4"'" 3 ....

3":

3 4-5"

3p

3 .... 3 ....

I ....

M. C Carbonell-Moore/Reviewof Palaeobotany and Palynology 84 (1994) 73-99

found on the bottom of the cingular plates of

Protoperidinium and related genera. He believed this finding would support Kofoid's assertion that the cingular plates had become fused to the precingulars and that the series of plates around the cell's equatorial plane were postcingular plates. However, similar pores are also found along the anterior sutures of most of the hypothecal plates, and are homologous to pores found along the bottom sutures of the precingular plates in some Podolampadaceans (Carbonell-Moore, unpubl. data). Indeed, similar pores on both the upper and lower sutures of the cingular plate can also be found in some Dinophysoids (cf. Hallegraeff and Lucas, 1988, figs. 14, 16). In Heterobractum (see below), the cingular plates are delineated by a single row of uniformly spaced pores (Plate IV, 6, 7). Ab6 (1966) related the antapical plates of Protoperidinium showing well-developed spines to the plates with spines in Podolampas. As Nie has described earlier, Ab6 also found four sulcal plates, although one of these was not a true sulcal plate either. Ab6's plate formula for the family Podolampadaceae was 3' la 5" 4S 3" 3p 3"". Balech (1963) related the three large plates found in the lower half of a Podolampadacean cell (Fig. 2A,B) to the three cingular plates found in Peridinioids. He determined that there were four true sulcal plates in the case of Blepharocysta and 4-5 in Podolampas. The plate that Nie and Ab6 termed a posterior sulcal plate was considered by Balech to be an antapical plate. Balech also referred to the spine-bearing plates as antapicals. According to Balech, the formula for the family Podolampadaceae was 3' la 5" 3C 4-5S 2-3" 3.... *. Carbonell-Moore (1991) redefined the genus Lissodinium Matzenauer, which had been, until then, an obscure genus included in the Lissodiniaceae family created by Schiller (1937) and revealed the similarities in the plate tabulation pattern of Lissodinium to Blepharocysta and Podolampas by applying Balech's plate formula for the family Podolampadaceae. Five sulcal plates and two of the apical pore plates were included in the formula for Lissodinium. *In some members of the Blepharocysta denticulata Nie complex, one of the postcingular plates is missing.

75

Balech's formula for the hypotheca is still not very satisfying because the antapical plates are situated ventrally in most Podolampadaceans. The anterior suture of the plates enclosing the sulcus (1 .... and 3"") is near the equator of the cell (Fig. 2B). Balech (1980) introduced the term "perisulcal" to designate those plates bordering the sulcus without being connected with the cingulum. This name would replace the name "antapical" as some "antapical" plates were not in antapical position at all. Nevertheless, in the Podolampadaceans the outer sutures of plates 1.... and 3"" are behind the cingular plates; hence the term "perisulcal" could not be applied in this case. In the three genera of the family Podolampadaceae, the postcingular plates are located on or near the cell antapex. Two of these plates have sutures simultaneously with the middle cingular plate and with either C1 or C 3. It is clear that a more logical plate designation of the hypothecal plates of the Podolampadaceans is needed. In this paper, the hypothecal plate formula of the family Podolampadaceae is redefined based upon the similarities of these dinoflagellates to another Peridinioid, i.e. Diplopsalis sensu Dodge and Toriumi (1993). This relationship is established on the grounds of homology comparisons of both the epithecal and hypothecal plate series. Two new Podolampadacean genera are described based upon the differences found in the apical pore plates or in the cell compression. A third new genus is proposed for those Podolampadaceans with a unique bilateral plate asymmetry. Finally, the relationships and possible evolutionary trends of the genera of the family Podolampadaceae are discussed.

2. Material and methods

Approximately 550 dinoflagellate cells from the family Podolampadaceae were isolated from samples collected from numerous oceanographic expeditions and examined under light and scanning electron microscopes. From the Atlantic, Gulf Stream, Colombian Caribbean, Southwestern Atlantic and Mediterranean samples were analyzed. Samples from the Pacific Ocean include

76

M. C Carbonell-Moore/ Review ~[ Palueobotany and Palynology 84 ( 1994i 73 99

Fig. 1. Diagram to illustrate the apical pore complex and apical plates of the Podolampadaceans as represented by Lissodinium (from Carbonell-Moore, 1993).

Central and Eastern Equatorial areas as welt as the Southwestern Pacific. From the Indian Ocean, samples from the Bay of Bengal were observed. The methodology followed has been described in Carbonell-Moore (1991, 1992, 1993).

3. Results and discussion

The apical pore complex (APC) of the Podolampadaceans is represented in Fig. 1. This is similar to the apical pore complex of most Peridinioids, which is formed by three plates (or platelets) described as pore, cover and canal plates (Dodge and Hermes, 1981 a). The pore plate refers

to the plate that surrounds the actual pore, which is covered by the cover plate. The canal plate is an elongated plate which connects the pore plate to the first apical plate. Balech (1974) designated the canal plate as plate " X " and the pore plate as "Po". It seems appropriate to designate here the cover plate as "P~" where " t " comes from the Latin tect, meaning cover or roof, which indicates the function of this plate. Three well-defined types of apical pore complexes showing differences mainly on the pore and cover plates were found in the Podolampadaceans. The first two types are observed in Blepharo~Tsta and in Lissodinium respectively. A third type includes the APC of non-previously described Podolampadacean cells (see below). A comparative study of apical pores from different dinoflagellates excluding the Podolampadaceans was made by Dodge and Hermes (1981a). One can see similarities in the Podolampadacean's apical pore plates to the ones tbund in Peridinioids. The pore plate is perforated in Lissodinium (Fig. 1: Plate I, 2) and more closely resembles the pore plate found in Glenodinium hallii Freudenthal and Lee and in Heterocapsa triquetra (Ehrenberg) Stein (cf. Dodge and Hermes, 1981a, figs. 4, 15D). In BlepharocTsta, the pore plate, is also perforated, but is uniquely crossed with multiple ridges between the pores (Plate I, 1). The height of these ridges varies whereas no ridges are found in Lissodinium's pore plate (Plate I, 2). There is an unusually large pore on the left side of the pore plate which is very noticeable in Blepharocysta (Plate I, 1), in some

PLATE t Apical pores in different Podolampadaceans (8: scale b a r = 2 p.m; t, 2, 4, 5.: scale b a r s = 5 pro: 3, 6, 7, 9 I1: scale bars= 10 pm).

1. 2. 3. 4. 5. 6. 7. 8. 9.

10. I l.

Blepharocvsta paulsenii. Gulf of Naples. Lissodinium australe. Southwestern Atlantic (from Carbonell-Moore, 1993). Mysticella striata. Equatorial Pacific. Podolampas~spinf[era. Equatorial Pacific. Gaarderiaangusta. Equatorial Pacific. Heterobractum striatum. Equatorial Pacific. Podolampasreticulata. Barbados. Podolampasbipes. Indian Ocean. Gaarderiaangusta. Southwestern Atlantic. Gaarderiaangusta. Holotype. Equatorial Pacific. Differentcell than 5 or 9. Gaarderiaa r m a t a . Holotype. Equatorial Pacific.

M. C. Carbonell-Moore/Review of Palaeobotany and Palynology 84 (1994) 73 99

77

PLATE I

•O

78

M.C. Uarbonell-Moore/ Review qf Palueobotany and Pulvnolo~y ~4 ~ 1994) 73 99

species of Lissodinium (Plate 1, 2) and in Mysticella (see below) (Plate I, 3). The canal plate is elongated in Blepharocysta and Lissodinium, and has a small protuberance running lengthwise along the middle part of the plate (Plate I, 1, 2). This canal plate is as elongated as the plate found by Dodge and Hermes (1981a) in Glenodinium, Protoperidinium, Diplopsalis, or Scrippsiella. Plates Po, 2' and 3' in Blepharocysta, Lissodinium and Mysticella (see below) show ridges along the inner edges (Plate I, 1-3) similar to those found in some species of Diplopsalis, Boreadinium (cf. Dodge and Hermes, t981b, figs. 5, 7, 10, 11 ), Oblea (cf. Lewis, 1990, fig. 14) or Scrippsiella (cf. Dodges and Hermes, 1981a, figs. 12; cf. Lewis, 1991, fig. 55). It is not clear if the apical pore complex in Podolampas has the same three plates found in other Podolampadaceans. Podolampas spinifera Okamura (Plate l, 4) and P. antarctica Balech have a well-developed "spine" supported by a wide base on a plate that in P. bipes Stein is single perforated (Plate I, 8) or in P. reticulata Kofoid is apparently absent (Plate I, 7). In most species of Lissodinium, the cover plate has a centrally positioned spine, which varies in length and width (Carbonell-Moore, 1993). In Mysticella (see below), the cover plate has also a well-developed spine (Plate I, 3, Plate II, 13). In Blepharocysta, the corresponding spine is reduced to a very small protuberance (Plate I, 1). In addition to the types of apical pore complexes ( APC ) observed in Blepharocysta, Lissodinium and Podolampas, another APC was observed in nonpreviously described Podolampadacean cells. In this case, the pore plate is also perforated, as found in e.g. Lissodinium. Instead of the spine located on the cover plate, there is a very long ridge transcribing the canal plate which is also perforated (Plate I, 5, 6, 9-11 ). Most of these cells are included in a new genus (Gaarderia) described below. A second new genus (Mysticella, see below) is proposed for cells like Blepharocysta striata Scht~tt which present an apical pore complex similar to that of Lissodinium (Plate I, 3), but include non-compressed or slightly dorso-ventrally compressed cells. A third new genus (Heterobractum, see below) is proposed for cells with an apical pore

complex similar to that of Gaarderia, but which lack bilateral plate symmetry (Plate I, 6). The plate tabulation pattern of a typical Podolampadacean is shown in Fig. 2A,B. Fig. 3 shows the epithecal plates of non-compressed and laterally compressed cells while the hypothecal plates are displayed in Fig. 2C. When the Podolampadaceans are related to Diplopsalis sensu Dodge and Toriumi (1993), it can be observed that, by plate homology, the same epithecal and hypothecal plates are found in the Podolampadaceans as in Diplopsalis (Figs. 4A l, 8A-M). In the precingular plate series of the Podolampadaceans there is one plate less than in the same plate series in Diplopsalis (Fig. 4A-t). This reduction in the number of plates results from the loss of one suture, although not the same suture in all Podolampadaceans. Suture losses are relatively rare events in dinoflagellates. When a suture is lost, all of the other sutures and plates remain in similar position as in the original genus (Taylor, 1980). In Lissodinium and Heterobractum. plate 1" can be derived from the loss of the suture between plates 1" and 2" in Diplopsalis (Fig. 4A-C). In this way, plates 2" and 3" in these Podolampadaceans are homologous to plates 3" and 4" in Diplopsalis, which are also located dorsally to the anterior intercalary plate (Fig. 4A-C ). In all other Podolampadacean genera (Fig. 4D-I) the suture loss occurs between plates 3" and 4" in Diplopsalis (Fig. 4A). In this way, there is only one plate dorsally connected to the anterior intercalary plate, which is then the homologous of the fusion of plates 3" and 4" in Diplopsalis (Fig. 4A, D-I). As a result, plates I" and 2" in these Podolampadaceans are homologous to plates 1" and 2" in Diplopsalis. Plates 4" and 5" in all Podolampadaceans are homologous to plates 5" and 6" in Diplopsalis (Fig. 4A-I). The loss of the suture between plates 1" and 2" in Diplopsalis as observed in Lissodinium and Heterobractum (Fig. 4A-C) results in the loss of the suture between plates 2' and 2" (Fig. 5D,C). This is showed in the long side of plate 2' in the left side of the cell (Fig. 4B,C). If we compare this plate with the homologous plate in other Podolampadaceans, i.e. Blepharocysta and Podolampas, one finds two sides of plate 2' on the

M. C Carbonell-Moore/Review of Palaeobotany and Palynology 84 (1994) 73-99 APC

C3

79

APC

C2

(

i C

NEW PLATE FORMULA

Po Pt X 3' l a 5" 3C 4-5S 4-5"' 1....

D OLD PLATE FORMULA

Po Pt X 3' l a 5" 3C 4-5S 2-3'" 3 ....

Fig. 2. Diagrams to illustrate the old and new formulas on the plate tabulation pattern of the Podolampadaceans as represented by

Blepharocysta. (A) Ventral view, new plate formula. (B) Same as (A), old plate formula. (C) Hypothecal plates, new plate formula. (D) Same as (C), old plate formula.

left side of the cell instead of one (these sides are the sutures with 1" and 2") (Figs. 4D,E,I, 5A). This is because in Blepharocysta or Podolampas, plate 1" is the homologue of only plate 1" in Diplopsalis. However, in Mysticella and Gaarderia, even though presenting the same loss suture found in Blepharocysta and Podolampas, plate 2' does not touch plate 2" (Fig. 5B) as it does in these last

two genera (Fig. 5A). As the precingular plate size increases, the apical plate size decreases (Fig. 4B-I). While plate 1' is large in Diplopsalis (Fig. 4A), in most Podolampadaceans it is very narrow and is easily overlooked (Fig. 4B,C,E-I). However, this plate is relatively wide in Blepharocysta hermosillai Carbonell-Moore (Carbonell-Moore, 1992) and in

80

M. C Carbonell-Moore/Review ~)/Palaeobotany and Palynology 84 ( 1994; 73 99

i

ll I b

II

Fig. 3. Diagrams to illustrate the epithecal plates in the Podolampadaceans. (A). A non-compressed cell, as represented by Blepharo~Tsta. (B) A laterally compressed cell, as represented by Lissodinium (from Carbonell-Moore, 1993l.

most of the species of the B. denticulata Nie complex (Carbonell-Moore, unpubl, data) (Fig. 4D). The development of the cingular plates in different Podolampadaceans is shown in Fig. 6. The sutures in this plate series with the postcingular plate series are not the same as in Diplopsalis. The long narrow C2 plate in Diplopsalis has sutures shared with three of the postcingular plates: 2'", 3'" and 4" (Fig. 6A). In the Podolampadaceans these sutures vary. In Mysticella striata (see below) the posterior side of C2 shares sutures mainly with 3"' and a short portion of 2" (Fig. 6B). A similar case occurs in Heterobractum, but instead of sharing short sutures with 2"', it shares the short suture with 4" (Fig. 6C). In other Podolampadaceans, plates 2"' and 4'" simultaneously share sutures with two cingular plates, either C2 and C~ in the case of 2' or C2 and C3 in the case of 4" (Fig. 6D J ). In the Podolampadaceans, the length and width of plate C2 is highly variable. In Mystycella striata (Fig. 6B), plate Cz is very narrow, and, as in Diplopsalis, has only four sides (Fig. 6A). In Heterobractum it has five sides (Fig. 6C). As the plate size increases two new sutures appear to better accomodate plates 2"' and 4'". This sixthsided plate is relatively narrow in Blepharocysta hermosillai (Fig. 6D), although in other species of Blepharocysta, e.g.B, paulsenii, it can increase considerably in size (Fig. 6E). In extreme cases, plate C2 entirely occupies the dorsal hypotheca,

e.g. Mysticella spinosa (see below) (Fig. 6G). Consequently, four of the postcingulars are located ventrally in this species (Plate II, 11 ). The relative size of the cingular plates also varies greatly. The three cingular plates in Mysticella striata (see below) and in Heterobractum are of the same size (Fig. 6B,C). Whereas in most species of Podolampas, Blepharocysta and Gaarderia and even Mysticella spinosa (see below) plate C1 is the smallest of the series (Fig. 6D,E,H,J), in P. bipes Stein, P. reticulata Kofoid and Lissodinium plates C1 and C3 are of similar size (Fig. 6E,I ). Four or five sulcal plates can be observed in the Podolampadaceae. Podolampas and Lissodinium have five (Balech, 1963; Carbonell-Moore, 1991), while all the other genera only present four (Fig. 7B,C). It is possible to see that the anterior sulcal (S.a.) in the Podolampadaceans is derived (Fig. 7B~C) from the fusion of the left sulcal (S.s.) and anterior sulcal plates of most Peridinioids (Fig. 7A). Similarly to the Peridinioids, the first apical plate lies adjacent to the sulcal anterior plate in the Podolampadaceans (Fig. 7B,C). The corresponding posterior sulcal (S.p.) and right sulcal (S.d.) plates of the Peridinioids are also found in the Podolampadaceans (Fig. 7A-C). In most Podotampadaceans **, the right sulcal plate **Exceptions are Lissodhzium and some species of the Blepharocysta denticulata complex Nie (Carbonell-Moore, 1993 I.

M. C. Carbonell-Moore/Review of Palaeobotany and Palynology 84 (1994) 73 99

~

A

~

D

E

81

C

iiiiiiiiI

i ~

I G 1" A,D-I

H

~ii~i~~i ~ii~ii~ii~,~

5" A 4"

B-I

2"

A, D-I

3"

A

~

4"

A

1"

B,C

2"

B-C

~

3"

B-I

~

6" A 5'"

B-I

.~

Apical plate series

1'- 3 A-I

Fig. 4. Diagrams to illustrate the epithecal plates in different Podolampadaceans as compared to Diplopsalis. (A) Diplopsalis lenticula. (B) Lissodinium taylorii. (C) Heterobractum striatum. (D) Blepharocysta denticulata. (E) Blepharocysta paulsenff. (F) Mysticella striata. (G) Gaarderia angusta. (H) Gaarderia armata. (I) Podolampas bipes. The dashed lines indicate the position of plate C1 in all the other species of Podolampas except P. reticulata.

82

M. C] Carbonell-Moore:'Revie~*" ol Palaeobolany and Palvm)logy ~4 i 1994i 73 9'9

la

la

:1" 2

/

.

2I

1 II

A

B

D

C

Fig. 5. Diagrams to illustrate the different apical sutures on the left side of the Podolampadaceans. (A) Blepharocysta and Podolampas. (B) Mysticella and Gaarderia. (C) l, issodinium. (D) Heterohracmm.

A P

~!!..:.:.:.:.:.:.::i:i:i:~iiiiiiii!i!i:~

....~ i l :i

B ,'iiJ i :ill

C

D

E 2

4'"

3'"

5"'

Fig. 6, Diagrams to illustrate the development of the cingular plate series m different t) odolampadaceans as compared to Dit~lol~sah's. (A) Diplopsali.~ lenticula. (B) Mysticella striata. (C) Heterobractum striatum. (D) Blepharocysta hermosillai. (E) Blepharocvsta paulsenii. ( F ) Lissodinium heteroporum. ( G ) Myst icella spinosa. ( H ) Po(h)lampas eleg,ans. ( I ) Podolampas hipes. ( J ) Gaarderia angusla.

M. C. Carbonell-Moore/Reviewof Palaeobotanyand Palynology84 (1994) 73-99 is very similar in shape to that in other Peridinioids. As found in Diplopsalis, the S.d. touches 1.... only in Podolampas (Figs. 8A,H,I). In all other Podolampadaceans the S.d. never touches 1.... (Figs. 7B,C, 8B-G,J-M). If one assumes that the three plates on the equatorial plane of a Podolampadacean cell (Fig. 2A,C) are the homologues to the three cingular plates of Diplopsalis and other Peridinioids, and one further assumes that the transitional plate " t " in these Peridinioids has fused with the anterior sulcal (S.a.) (Fig. 7A), then the five plates in contact with these three cingular plates could be considered as postcingulars (Fig. 2A,B). These five plates would then be homologous to the five postcingulars found in Diplopsalis (Fig. 8A-M). If the plates laying posteriorly to the cingular plates are postcingulars, then there would be only one antapical plate, located on or near the antapex. Diplopsalis has only one antapical plate (Fig. 8A) which then is homologous to a much smaller plate found in all Podolampadaceans (Fig. 8B-I). The plate formula for the hypotheca of the Podolampadaceans would be written as 5"' 1.... instead of 3 .... 3 .... as suggested by Balech (1963) (Fig. 2C,D). Fensome et al. (1993) also found five

83

postcingular plates based upon overlapping plate studies. A reduction in plate size can be observed in the antapical region similar to the reduction described earlier in the apical region. In Diplopsalis the 1"" plate is very large while the cingular plates are very narrow. It can be said that by enlarging the cingular plates, the postcingular and antapical plate series necessarily decrease in size. Plate 1"" is greatly reduced in most species of Blepharocysta and in Podolampas and has been confused by some authors with a sulcal plate (Fig. 8D,E,H,I). Developed lists in the Podolampadaceans are commonly found along the inner edges of 1" and 5" plates, e.g. Blepharocysta. In some cases, as found in Diplopsalis (Figs. 6A, 8A) the left list is much larger than the right one. This list is represented by a reinforcement, e.g. in Podolampas and Mysticella spinosa (Plate lI, 11). Plate l .... may contain a narrow list in Podolampas and in some species of Blepharocysta, such as B. hermosillai Carbonell-Moore. As pointed out by Ab6 (1966), spines on Protoperidinium are located on the antapical plates. In Podolampas, well-developed spines are found on 1" and 5" plates. The presence of antapical spines in the family Podolampadaceae is

|1

)

...,

3 III

A

B

S.p.

C

Fig. 7. Diagrams to illustrate the plates of the two types of sulcal region of the Podolampadaceanscompared to Diplopsalis. (A) Diplopsalis(modifiedfrom Dodges and Hermes, 1981b). (B) Gaarderia.(C) Lissodinium(from Carbonell-Moore, 1993).

84

M. C. C'arhonelI-Moore/ Review qf Palaeohomny aml Palvnoh~gy h'4 f 1994; 7j 09

A

c2

1 G

J

~

K

(;ingLl I i~ pl slrate~e r iP pal°estctniegseri ualress

L

M

1'"'plate~

NIJl plaeta'eSeries

Fig. 8. Diagrams to illustrate the hypothecal plates of different Podolampadaceans as compared to Dil~lopsalis, (A) Diph~psalis lenticula. (B) Mysticella striata. (C) Blepharocysta hermosillai. (D) Blepharoc.vs'la okamurai. /E) Blepharocysta denticulata. (F) Lissodinium taylorii. (G) Heterobractum strkttum. (H) Po~k)lampas hipes, l l) Po~hdampas elegant'. (J) Gaarderia angusta, Cell with no compression. (K) Gaarderia angusta. Cell slightly compressed. (L) Gaarderia lata. Cell with almost total lateral compression. (M) Gaarderia armam. Laterally compressed cell.

M. C Carbonell-Moore/Reviewof Palaeobotany and Palynology 84 (1994) 73-99

no longer a feature unique to Podolampas. Besides Mysticella spinosa (see below), two species of Lissodinium show antapical spines. These spines are not associated with lists and are not as welldeveloped as those seen in Podolampas (CarbonellMoore, 1993). Thus, some Podolampadaceans are within the few dinoflagellates that, according to Taylor (1987), present spines. Another feature common to most Podolampadaceans is the elaborate zone of honey-combed pores on plate 1"" observed in Gaarderia, Mysticella, Heterobractum (see below), and some species of Lissodinium (Carbonell-Moore, 1993). This honey-combed zone may be raised in Mysticella spinosa (PlateII, 11, 12, 14) or in Gaarderia armata (Plate IV, 4, 5). The function of this zone of honey-combed pores is unknown. Similarly, in Blepharocysta there are some very large pores on 1.... (Plate II, 3) inspite of the small size of this plate. In Podolampas, there are two rows of round pores following a unique pattern along the postcingular plates not found in any other Podolampadaceans (Carbonell-Moore, 1991). A very interesting feature of the Podolampadaceans is the broad range of compression displayed by the cells. Blepharocysta has almost no compression at all (Fig. 4D,E), and most Podolampas species are dorso-ventrally compressed (Fig. 4H,I). In Lissodinium the lateral compression is perpendicular to the dorso-ventral axis of the cell (Fig. 4B). In Gaarderia it is possible to see oblique compression at approximately 45 degree angle to the dorso-ventral cell axis (see below). This oblique compression alters the cell's bilateral symmetry. The different degrees of compression are illustrated in Fig. 8J-M. In the type species Gaarderia angusta (see below) this distortion is minimized (Fig. 8J,K). It becomes maximized in G. armata (see below) (Fig. 8M). Mysticella spinosa (see below) is slightly dorso-ventrally compressed (Plate II, 13) and is deeply depressed along the mid-ventral part of the cell (Plate II, 11 ). The biology of the Podolampadaceans is not well known. The presence of numerous zygotic forms, i.e. large cells with enormous intercalary bands (Pfiester and Skvarla, 1979) suggests that sexual reproduction occurs in the

85

Podolampadaceans. Carbonell-Moore (1993) found that these zygotic stages were fairly common in two species of Lissodinium and suggested that they may correspond to planozygotes. In the present study, numerous planozygotic forms, as the ones in Plate II, 1-3, were observed in only a few species. As in the case of Lissodinium, the larger the planozygote, the smaller the size of the plates. None of these zygotic forms have yet been seen in any of the species of Podolampas. Additionally, numerous very small cells of some species of Podolampas were observed in the present study. This may also be an indication of sexual reproduction. According to Pfiester and Anderson (1987) and MacKenzie (1992), smaller cells of a certain species occurring in culture or in wild populations are gametes. Hallegraeff and Jeffrey (1984) determined under the fluorescence microscope that Podolampas and Blepharocysta are non-photosynthetic. Observations by SchOtt (1895) on Mysticella striata, and by Steidinger and Williams (1970) on Blepharocysta splendor-maris (sensu these authors) indicate that the Podolampadaceans may feed by a mechanism similar to other heterotrophic dinoflagellates. These dinoflagellates feed externally by means of a "veil, or pallium" that is extruded through the flagellar pore and envelops the prey (Gaines and Elbr/~chter, 1987). The prey is then liquified inside the pallium so no food particles can be seen being transported to the theca (Jacobson and Anderson, 1992). A similar pallium can be observed in Scht~tt (1895, figs. 61.10-16, 61.19) and in Steidinger and Williams (1970, figs. 9a,b). The Podolampadaceans show a similar geographic distribution and the different genera tend to coexist; they are more abundant between 100-200 m, showing a wide range in both vertical and latitudinal distribution with a maximum species diversity found in the tropics (CarbonellMoore, 1994, this issue). A clear evolutionary trend within the family is difficult to discern from the great diversity of features observed in the Podolampadaceans. It can be said though, that Diplopsalis seems a probably common ancestor from which at least Lissodinium, Blepharocysta and Mysticella might have derived.

M.C. CarbonelI-Moore/Review q/'PalaeobotaLv and Palynology 84 I 1994,J 73 99

86

PLATE ll

M. C. Carbonell-Moore/Review of Palaeobotany and Palynology 84 (1994) 73 99

As seen earlier, Podolampas might be closely related to one species of Mysticella but if both the cingular and sulcal plates are considered, it is closely related to Diplopsalis. Heterobractum, although apparently with an epithecal and a cingular plate series similar to those Mysticella, shows a very unique assymetry in the hypothecal plates, that cannot yet be related to any other genus in the family. On the other hand, the epitheca's plate symmetry is similar to that in Lissodinium. Challenging studies involving the biology of the family await for a better understanding of the taxonomy of this diverse group.

4. Taxonomy MYSTICELLA Carbonell-Moore, gen.nov. Type: Mysticella striata (SchtRt, 1895) CarbonellMoore, comb. nov. Diagnosis: Cellulae ovoideae cingulo bene circumscripto carentes; sulcus longus uno uel duobus membranis magnis in¢lusus. Cellulae aut dorsoventraliter compressae aut compressione carentes. Spinae in antapice fortasse adsunt. Lamina apicalem tegens cum spina bene definita latitudine basis aequo ad laminae diametrum. Lamina pori apicalis cum multiplicibus perforationibus approximatis. Lamina

2' et 3' nec dorsaliter nec ventraliter tangentes. Formula laminarum." Po Pt X 3' la 5" 3C4S5"' 1"". The ovoid cells are lacking a well-defined cingulum. The long sulcus is enclosed by one or two large lists. Cells are either dorso-ventrally compressed or are lacking compression. Spines might be present on the antapex. The apical pore plate has multiple regularly-spaced perforations. The apical cover plate has a well-defined spine whose base's width equals the plate's diameter. Plates 2' and 3' do not touch either dorsally nor ventrally. Plate formula: Po Pt X 3' 1a 5" 3C 4S 5" 1"". Etymology: The name chosen for this genus refers to the "mystery" (from Greek myst = mystery) that has surrounded the type species since it was first described by Schtitt in 1895 as a species of Blepharocysta (see below). Discussion: The thecal characteristics of this genus represent a combination of features found in other genera in the Podolampadaceans. The cover plate with its spine resembles the apical pore complex found in Podolampas spinifera and P. antarctica. The apical pore plate is similar to that found in Lissodinium. The general plate arrangement is similar to Blepharocysta's, but differs mainly from it in the characteristics of the apical pore complex. The anterior intercalary plate has a boomerang shape with five sides and not four as in Blepharocysta.

PLATE II 1 3.

Planozygotes of different Podolampadaceans. Mysticella's planozygote. Equatorial Pacific (scale bar = 20 lam). Gaarderia'splanozygote. Gulf Stream (scale bar = 50 Ixm). Blepharocysta's planozygote. Equatorial Pacific. (scale bar = 20 ~rn). 4-10. Mysticella striata (4, 7, 9, 10: scale b a r s = 2 0 ~tm; 8, scale b a r = 10 ~tm). 4. Same cell as Plate I, 3. Equatorial Pacific. Ventral view. 5. After SchOtt (1895). Right-lateral view. 6. Same as 5. Apical view. 7. Same cell as 4. Dorsal view, showing the narrow C2. 8. Same cell as 4. Antapical view. 9. Same cell as Plate I, 3. Right-lateral view. 10. Same cell as 4. Apical view. 1 l-14. Mysticella spinosa (11, 12: scale bars = 20 ~rn; 13, 14: scale bars = 10 p_m). 11. Holotype. Ventral view. Equatorial Pacific. 12. Different cell. Equatorial Pacific. Dorsal view. 13. Same cell as 11. Apical view. 14. Same cell as 12. Antapical view, illustrates the sharp spine on plate 1"'.

1. 2. 3.

87

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M.C. CarbonelI-Moore:Review o/Palaeobotanv and Palym)logy 84 : 1994:73 q9

One new combination is proposed and a new species is described.

Mysticella striata (Schatt, 1895) Carbonell-Moore, comb. nov. (Plate I, 3; Plate II, 4 10; Figs. 4F, 6B, 8B) Basionym: Blepharocysta striata Schfitt, 1895, Ergeb. Plankton-Exped. Humboldt-Stiftung, 4: 162, plate 20, 59.1 59.10. Schtitt, 1896, p. 24, 34c. Rampi, 1941, p. 149, plate 5, 7. Gaarder, 1954, p. 8. Description: Ovoid, medium-sized non-compressed cell. Distinctive elongated apical pore complex (APC), consisting of three plates. The pore plate is oval and has many closely-spaced perforations (Plate I, 3). There is a much larger pore on the left side of this plate (Plate I, 3). A ridge extends along the inner edge of the pore plate. The cover plate has a well-developed spine whose base extends dorso-ventrally almost the entire length of the plate. The canal plate, which has a very small protuberance, meets plate 1' posteriorly. Plates 2' and 3' are symmetrical and embrace the APC although their anterior and posterior ends are slightly separated (Plate|, 3). Plate2' is threesided whereas plate 3' is four sided (Plate I, 3).

Plate 1' is very narrow (Plate l, 3: Plate II, 10). The anterior intercalary plate has six sides, boomerang-shaped; the boomerang vertex is located between plates 2" and 3" (Plate I, 3). The precingular plates are similar in size (Plate II, 10). Cingulars are unusually narrow, and because of this, plates 2"', 3"' and 4" are as wide and as long as the precingulars. Plates 1"' and 5'" are also long but are narrower (Plate I l, 4, 7 9 ) . Plates 1'" and 5"' bear long and wide lists (Plate II, 4, 8). The antapical plate is very large with honey-combed pores that cover almost the entire plate surface (Plate II, 8 ). Under the SEM the thecal pore array of most plates consists of alternate elongated and small round pores in an almost perfect alignment (Plate II, 4, 9, 10). The pore arrangement is best delineated on the epithecal plates. The hypothecal plates do not show it in the specimens observed in this study. Plate C~ has far fewer pores than any of the other thecal plates (Plate II, 7). Total length: 50.6 56.9 ttm. Dorso-ventral axis: 37.3 38.5/Lm. Lateral axis: 37.5 46.6 l~m. Discussion: The cingular plates are unusually narrow when compared to most Podolampadaceans (Fig. 6B; Plate ll, 4, 5, 7, 9). As mentioned earlier, Schtitt (1895) was the first to

PLATE Ill Gaarderm angusta ( 1 4, 8: scale b a r s = 2 0 lain: 5, 6: scale b a r s - 10 ~am: 7: scale b a r = 5 !-roll, Holotype. Same cell as Plate I, 10. Ventral view. Equatorial Pacitic. 1. Same cell as Plate l, 9. Southwestern Atlantic. Ventral view. 2. Different cell, Apical view. Equatorial Pacific. 3, Same cell as 2. Apical view. 4. Different cell, Antapical view. Equatorial Pacific. 5. Same cell as 5. Ventral view. 6. Holotype. Same cell as 1. Lower ventral view. 7. Different cell, Right-lateral view. Equatorial Pacific. 8. 9 14. Gaarderia lata (scale b a r s = 10 l,tm). Holotype. Apical view. Gulf Stream. 9. Holotype. Same cell as 9. Right-lateral view. 10. Holotype. Same cell as 9. Right-ventral view. 11. Different cell. Dorsal view. Southwestern Atlantic. 12. Same cell as 12. Antapical view. 13. 14 -19. Gaarderia compressa (scale b a r s - 10 lain). Holotype. Right-lateral view. Equatorial Pacific. 14. Holotype. Same cell as 14. Ventral view. 15. Holotype. Same cell as 14. Apical view. 16. Different cell. Left-lateral view. Equatorial Pacific, 17. Holotype. Same cell as 14. Antapical view. 18. Holotype. Same as 14. Dorsal view. 19, 1 8.

M. C. Carbonell-Moore/Reviewof Palaeobotany and Palynology 84 (1994) 73 99

P L A T E III

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PLATE

1 5. I. 2. 3. 4. 5. 6 9. 6. 7. 8. 9.

1994) 73 99

IV

Gaarderia armata. Holotype. Equatorial Pacific. Same cell as Plate I, 11 (scale bars=20 ~m). Apical view. Ventral view. Dorsal view. Right-lateral view. Antapical view. Heterobractum striatum. Holotype. Equatorial Pacific (scale bars=20 pin), Ventral view. Dorsal view. Antapical view. Right-lateral view.

M. C. Carbonell-Moore/Reviewof Palaeobotany and Palynology 84 (1994) 73-99

characterize these plates as cingulars. The sulcus if formed by four plates of similar shape to those in most species of Blepharocysta splendor-maris (Ehrenberg) Stein complex (Carbonell-Moore, unpubl, data). Similar enlarged pores to the ones found on the antapical plate of Mysticella striata have also been observed on the same plate in some species of Lissodinium (Carbonell-Moore, 1993) and in Gaarderia (e.g. Plate lII, 7). Schtitt's illustration indicates the characteristic "striated" thecal pore arrangement on most of the plates, which gave the name to the species (Plate II, 5, 6). Similar pore arrangements can also be observed in other Podolampadacean cells (Plate III, 3, 16; Plate IV, 3). This species was originally described by Schiatt during the Plankton Expedition across the Atlantic, which covered boreal and tropical waters. Schtitt provided very detailed illustrations of the cell in apical (Plate II, 6) and right lateral view (Plate II, 5) as well as details of the cell's interior (not shown here). Complete information on the antapex was not given. Schtitt only observed one living cell and this might have been all the material he observed of this species. Other earlier reports in the literature include Rampi (1941) who observed a few cells in dorsal view from the Ligurian Sea. Due to the characteristic pore plate pattern of Mysticella striata as described by SchOtt, Rampi identified his specimens as this species. Because of his limited dorsal view of the specimens, his identification remains uncertain. Gaarder (1954) found a single specimen in a 0-1000 m sample during the North Atlantic Expedition, but no illustration accompanied this report. This author found several cells in the present study in the Equatorial Pacific (0°140°W) between 100 and 200 m. The total length of the cell depicted by SchOtt is 41 #m as calculated from his illustration, somewhat smaller than the specimens observed here.

Mystieella spinosa Carbonell-Moore, sp. nov. (Plate II, 11-14) Holotype: Plate II, 11, 13. Total length: 45.5 #m. Dorso-ventral axis: 27.0/zm. Lateral axis: 38.3 #m. SEM specimen No. 384, kept at Oregon State

91

University, College of Oceanic and Atmospheric Sciences, Corvallis, OR, USA. Type locality: Equatorial Pacific 0°140°W found between 150 and 200 m. Etymology: Its name refers to the spines found on plate 1.... and on the lower edge of the sulcal membrane of plate 1". From Latin spina = spine. Diagnosis: Cellulae leviter pyriformes, dorsoventraliter compressae, antapice asymmetrico et depressione longa in medio parte ventrale. Complexum pori apicalis inclusum altis extensionibus laminarum 2' et 3' brevem collum formantibus. Hae extensiones poris carentes. Membrana sulci laevi amplificata, spinam in extremo; lamina 1"" cure spinam acutam et zonam extrusam pororum favosorum habet. Formula laminarum: Po Pt X 3' la 5" 3C 4S 5" 1"". The slightly pear-shaped cells are dorso-ventrally compressed, with an asymmetric antapex and a long depression in the middle ventral part of the cell. The apical pore complex is enclosed by very tall extensions of plates 2' and 3', that form a short neck. These extensions lack pores and are thickly reinforced. Enlarged left sulcal list bears a spine on the lower end. Right sulcal list is reduced to a narrow reinforcement. The antapical plate contains a sharp spine and a extruded zone of honeycombed pores. Plate formula: Po Pt X 3' la 5" 3C 4S 5" 1"'. Description: Slightly pear-shaped, dorso-ventrally compressed cells, with an asymmetric antapex and an elongated depression along the mid-ventral part of the cell (Plate II, 11). The apical pore complex is enclosed by very tall extensions of plates 2' and 3' which form a short neck (Plate II, 11, 13). These extensions lack pores and are thickly reinforced (Plate lI, 11). The cover plate bears a welldeveloped spine (Plate II, 13). The wide anterior intercalary plate is boomerang-shaped (Plate II, 13). The base of plates 2' and 3' is narrow and covered with small pores (Plate II, 13). Precingular plates 1", 2", 4", 5" are relatively symmetrical, whereas 3" is much wider and occupies the entire dorsal epitheca (Plate II, 12). Plates Ca and C3 are narrow (Plate II, 11), C1 shorter than C a. Plate C2 is very wide and occupies almost the entire dorsal half of the cell (Plate II, 12). The long sulcus is formed by four plates; the anterior and

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M.('. Carbone/l-Moore;Review q/ Palaeobotany and Palvnoh)~y ,~4 ( 1994.~ 73 99

right sulcal plates are narrow, while the U-shaped posterior sulcal plate is wide at the base (Plate II, 11). The medial sulcal plate has wide reinforcements which encircles the ventral opening (Plate |I, 11). Plate 1"' supports a long and wide list with a short spine at the lower end (Plate I], 11, 14). Plate 5"' is reinforced along the sulcus (Plate II, 11). Plate 3'" is curved and narrow (Plate II, 12, 14). On the left side of plate 1.... there is a slightly raised zone of honey-combed-like pores with a sharp spine at the far left end (Plate II, 14). Small round pores are present on the thecal plates. Elongated pores can also be found on some epithecal plates (Plate II, 11). Total length: 45.5 49.0 #m. Dorso-ventral axis: 27.0 28.2 t~m. Lateral axis: 38.3 40.6 ILna. Discussion: This species is closely related to some species of Podolampas, i.e.P, bipes Stein and P. reticulata Kofoid. In Mysticella spinosa the tall carina surrounding plates 2' and 3' enclose an apical pore complex bearing a very well-developed spine (Plate II, 11, 13). This carina resembles an elongated neck as in Podolampas, although not as long as in this genus. Mysticella spinosa shows an antapical spine on plate l .... and another spine at the lower end of the left sulcal list (Plate II, 1 l, 12, 14). The right sulcal list in both Mystieella ,spinosa and in Podolampas, is only a reinforcement (Plate II, 11 ). The relative size of the precingular plates in M. spinosa is similar to the one seen in those dorso-ventrally compressed species of Podolampas. Finally, a row of uniformily distributed pores can be seen along the edges of plate 3"' in MI spinosa (Plate I1, 12). These pores are different than other pores on the same plate. This row of pores is reminiscent of characteristic rows observed by Podolampas. The main differences between Mysticella spinosa and M. striata are: (1) Mysticella spinosa is dorso-ventrally compressed (Plate lI, t2, 14), while M. striata shows little compression (Fig. 4F; Plate 1I, 10~. (2) The edges of the carine along plates 2' and 3' in Mysticella ~v~inosa (Plate II, 11, 13 ) are thicker and the carine is taller than they are in M. strhm~ (Plate lI, 4, 10). (3) Hypothecal spines are present in Mysticella spinosa (Plate II, 11, 12, 14). No spines are found in Mysticella striata (Plate II, 4, 5, 7 9).

(4) Plate C 2 in Mysticella ,Vmlosa is very wide while plates C~ and C~ are narrow (Plate II, 11, 12). All cingular plates in Mvslieella striata are narrow (Plate II, 4, 5. 7, 9 ). (5) Plate l .... shows a raised zone of honeycombed pores with a spine in Mvsticella spinosa (Plate II, 14). In Mvstieella striata the zone of honey-combed pores is larger, not raised and lacks spines (Plate II, 8).

GAARDERIA Carbonell-Moore, gen. nov. 7),pc: Gaarderia angusta Carbonell-Moore, sp. nov. Diagnosis: Cellulae ovoideae vel lapill([brmes asvmmetrieae cingulo bene circumseripto carentes, sulcus hmgus duobus magnis membranis" inclusus. Cellulae leviter usque ad valse bilateraliter ao,mmetricae quod ab eompressione obliqua eellularum eff'eetum est. Lamina 2' et 3' dorsaliter tangentes. Lamina pori apicalis eum multiplieibus per/brationibus approximatis. Crista larga hene evoluta secus laminam canalem. Lamina l .... zona propria pororum Javosorum in laminae parte laeva locata. Formu]a laminarum: Po Pt X 3' la 5" 3C 4S 5'" 1"". The ovoid to asymmetric pebble-shaped cells lack a well-defined cingulum. The long sulcus is enclosed by two large lists. Cells are slightly to strongly bilaterally asymmetrical due to an oblique cell compression. Plates 2' and 3" touch dorsally. The apical pore plate has multiple, closely spaced perforations. A long, well-developed ridge is situated along the canal plate. Plate 1.... with a characteristic zone of honey-combed like pores is located on the left side of the plate. Plate formula: Po P~ X 3' la 5" 3C 4S 5'" I"". Etymology: Named alter Dr. Karen R. Gaarder from University of Oslo, Norway, author of numerous publications, among which, Dino,flagellatae .[i'om the "Michael Sars" NorthAthmtic Deep-Sea Expedition 1910 provided a broad knowledge on the distribution and taxonomy of Podolampadaceans. Discussion: The oblique cell compression along with a distinctive apical pore complex in this genus represent special features not found in other genera of the family Podolampadaceae. The cell bilateral asymmetry is very unique, especially in the extreme

M.C. Carbonell-Moore/Reviewof Palaeobotanyand Palynology84 (1994) 73-99

cases of cell compression. Four new species are described. Gaarderia angusta Carbonell-Moore, sp. nov. (Plate I, 5, 9, 10; Plate III, 1-8; Figs. 4G, 6J, 8J,K) Holotype: Plate I, 10; Plate III, 1, 7. Total length: 43.2 #m. Dorso-ventral axis: 33.0 #m. Lateral axis: 30.5 #m. SEM specimen No. 295, kept at Oregon State University, College of Oceanic and Atmospheric Sciences, Corvallis, OR, USA. Synonym: Blepharocysta sp., McKenzie, 1985, p. 251, plate 51, a-f. Type locality: Equatorial Pacific, 0°140°W, found between 150 and 200 m. Etymology: The narrow plates C1 and Ca give the name to this species. From the Latin angust= narrow. Diagnosis: Cellulae ovoideae leviter et lateraliter compressae, crista bene evoluta secus Pt and X. Laminae C1 and C3 angustae sunt. Formula laminarum." Po Pt X 3' la 5" 3C 4S 5" 1"'. The ovoid cells are slightly laterally compressed and have a well-developed ridge along Pt and X. Plates Ca and C3 are narrow. Plate formula: Po Pt X 3' la 5" 3 C 4 S 5" 1"". Description: The ovoid cells are laterally slightly compressed and have an elongated depression along the mid-ventral part of the cell (Plate III, 1). Round apical pore complex; Po has multiple perforations; Pt has a well-developed ridge that runs dorso-ventrally along both Pt and X (Plate I, 5, 9, 10; Plate III, 3, 4). Plate 2' is three-sided and plate 3' four-sided, both support a high ridge along the inner side (Plate I, 5, 9, 10; Plate III, 1-4, 6, 8). The anterior intercalary plate is boomerangshaped, with six sides, and points ventrally (Plate I, 5, 9, 10; Plate III, 3, 4). Plate 1' is very narrow (Plate I, 9, 10; Plate II, 6, 7; Plate III, 1, 2, 4). Plate 1" is narrower than the other precingulars. Plates Ca and C3 are narrow (Plate III, l, 2, 6). Plate C2 is very wide, long, and almost reaches the antapex (Plate III, 8). The sulcus is long and is formed by four plates among one is a very large and porosed posterior sulcal plate (Plate III, 7). Plates 1" and 5" are narrow, long, and both support large and evenly located fins (Plate III, 1, 2, 5-8). Plate 2" is also long and narrow (Plate III,

93

5-7). Plate 3" is narrow and slightly curved, and is located on the cell antapex (Plate III, 5, 7). Plate 4" is the largest of the postcingular plates (PlateIII, 1, 2, 5, 8). Plate 1.... is a large plate located near the cell antapex (Plate III, 5, 7, 8). On the left side there is a distinctive zone of honeycombed pores which on the micrographs appears much lighter in color than the rest of the theca (Plate III, 5, 7). The epithecal plates have alternating elongated and round pores forming almost straight lines from the apex to the cell equator (Plate I, 10; Plate III, 3, 6). Gaarderia angusta was found in the Equatorial Pacific, 0°140°W, mostly between 150 and 200 m. A few cells were also observed between 100 and 150 m. This species was also observed in the Southwestern Atlantic 50°23.8'S 40°56.3'W and 49°38.4'S 41°53.3'W. In cells from the Equatorial Pacific, plates 2' and 3' are asymmetrical (Plate I, 10), while in cells from the Southwestern Atlantic these plates are symmetrical (Plate I, 9). Total length: 36.9-49.7/~m. Dorso-ventral axis: 27.2-41.1/~m. Lateral axis: 25.6-41.6 #m. Discussion: The main feature that makes this species different from the other species described for this genus are the narrow cingular plates Ca and C3, and a much less pronounced lateral compression than that observed in all other species of Gaarderia. The zone of honey-combed pores on plate 1.... is not as raised as in Gaarderia armata or in G. compressa. The sulcal lists in Gaarderia angusta are evenly located (Plate III, 1) while in the other species especially in G. compressa, they are uneven (Plate III, 15). Thecal plates with elongated and round pores are arranged somewhat similarly to those found in other species of Gaarderia and Mysticella. Gaarderia lata Carbonell-Moore, sp. nov. (Plate III, 9-13; Fig. 8L) Holotype: Plate lII, 9-11. Total length: 35.8 pm.

Dorso-ventral axis: 38.8 pm. Lateral axis: 34.4 pm. SEM specimen No. 98, kept at Oregon State University, College of Oceanic and Atmospheric Sciences, Corvallis, OR, USA. Type locality: Gulf Stream 38°N 69°W. Etymology: The wide plates Ca and C3 give the

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M. C. Carbonell-Moore/Review o[ Palaeobotany and Palynologv 84 ~ 1994) 73 99

name to the species. From Latin latus=broad, wide. Diagnosis: Cellulae ovoideae leviter et lateraIiter eompressa. Laminae 1" et 4" angustiores quam alterae laminae precingulares. Laminae C1 and C 3 latae sunt. Latus laevum laminae 3"' curvature sed dextrum rectum est. Latus laevum laminae 1 .... dextro brevius. Pori laminae epithecae elongati, rectilineares et parvis poris rotundis alternantes. Formula laminarum: Po Pt X 3' la 5" 3 C 4 S 5 ' " 1"". The ovoid cells are slightly laterally compressed. Plates 1" and 4" are narrower than other precingulars. Plates C~ and C3 are wide. Left side of plate 3"' is curved whereas the right side is straight. Left side of plate 1.... is shorter than the right side of the plate. Epithecal plate pores elongated, aligned and alternated with small round pores. Plate formula: Po Pt X 3' la 5" 3C 4S 5'" 1'"'. Deseription: The ovoid cells are slightly laterally compressed (Plate III, l 1). The apical pore is similar to the type species (Plate IlI, 9~. Plates 2' and 3' are symmetrical with a tall ridge along the inner sides that meets dorsally (Plate III, 9). Plates 1" and 4" are narrower than the other precingulars (Plate III, 9). Plates C~ and C3 are wide (Plate III, 10, 11 ). Plate C: is very large (Plate III, 12). The right side of plate 3"' is straight, whereas the left side is curved (Plate IIl, 13). The right side of plate 1"" is shorter than the left side which displays a zone of honey-combed pores as in the type species. These pores are raised in some specimens (Plate IlI, 13). Epithecal plate pores are aligned such that elongated pores alternate with small round pores (Plate III, 9). Large round pores are found on other plates (Plate III, 10). Also found in the Southwestern Atlantic 50°S 4 1 W , in the Equatorial Pacific 0:I40°W and in the Coral Sea 17'S 152~E. Total length: 35.8-49.7 #m; dorsoventral axis: 31.0 34.0 #m; lateral axis: 34.4 43.6 #m. Megacytic cells may be as 59.0 l~m long and 47.0 #m wide. Discussion: Gaarderia lata is closely related to G. angusta and the main differences between the two species can be summarized as follows: (1) In Gaarderia lata all cingular plates are much wider (Plate IlI, 10- 12) than in Gaarderia angusta (Plate lII, 1, 8). (2) There is much more cell asymmetry in

Gaarderia lata (Plate Ill, 9) as a consequence of a more pronounced cell compression that in G. angusta (Plate IlI, 4) but not as much as in Gaarderia compressa (Plate III, 16) or in G. armata (Plate IV, 1 ). Gaarderia lata is also more distorted (Plate lIl, 11 ) than G. angusta (Plate III, 2). (3) Plate3" is narrower in Gaarderia lata (Plate IIl, 12) than in G. angusta (Plate III, 3). (4) The right side of plate 3'" is straight whereas the left side is curved in Gaarderia lata (Plate II1, 13). In Gaarderia angusta both sides are curved (Plate Ill, 5). Gaarderia compressa Carbonell-Moore, sp. nov. (Plate III, 14 19) Holoo,pe: Plate III, 14 16, 18, 19. Total length: 29.2 #m. Dorso-ventral axis: 31.9 #m, Lateral axis: 21.5 #m. SEM specimen No. 337, kept at Oregon State University, College of Oceanic and Atmospheric Sciences, Corvallis, OR, USA. Type locality: Equatorial Pacific 0~140~'W, found between 150 and 200 m. Etymology: The cell's pronounced lateral compression gives the name to the species. From Latin compressus = flattened. Diagnosis: Cellulae minutae, lapilliJbrmes et lateraliter compressae, latere ventrale acutissimo et latere dorsale leniter curvato. Crista longissima in lamina X dimidium intervalli ad bracteas cingulares producens. Latus postieum laminae anticae intercalaris brevissimum. Laminae C2 and C3 grandissimae: lamina C1 lateraliter angustus. Laminae 2'" et 3' angustissimae. Formula laminarum: Po Pt X 3' la 5 " 3 C 4 S 5 ' 1"". The pebble-shaped, small, laterally compressed cells, have a very pointed ventral side and a gently curved dorsal side. The very long ridge on the X platelet reaches almost midway to the cingular plates. The posterior side of the anterior intercalary plate is very short. Plates C2 and C3 are very large; plate C~ is narrow laterally. Plates 2'" and 3'" are very narrow. Plate formula: Po Pt X 3' la 5" 3C 4S 5'" I"". Description: The small, pebble-shaped, laterally compressed cells have a very pointed ventral side and a gently curved dorsal side (Plate III, 14, 17) and a large apical pore complex (Plate II1, 16).

M. C. Carbonell-Moore/Reviewof Palaeobotany and Palynology 84 (1994) 73-99

The very long ridge on the X platelet reaches almost half-way to the cingular plates. The posterior side of the anterior intercalary plate is very short, resembling a truncated boomerang with one side much longer than the other (Plate III, 16). Plate 1" is the narrowest plate in the precingular series whereas plates 2" and 5" are the widest. Dorsal plates 3" and 4" are asymmetrical, plate 4" is much larger than 3". Plate C1 is narrow and short (Plate III, 15). Plate C2 occupies almost the entire lower left side of the cell (Plate III, 17). Plate C3 is as long as C2 but narrower (Plate III, 14). Plates 2"' and especially 3"', are very narrow and long (Plate III, 15, 18). Plates 1" and 5"' support large lists (Plate III, 14, 15, 18). Plate 1.... is large and supports a small zone of honeycombed pores which is slightly raised on the thecal plate surface (Plate lII, 17, 18). The epithecal plates are covered with aligned large elongated pores (Plate III, 16). This species is distinctively shaped and identifiable under the light microscope. Total length: 29.2-43.6pm; dorso-ventral axis: 31.9-42.7/~m; lateral axis: 20.9-28.8pm. Also found at 5°N 140°W at the same depth of the holotype. Discussion: This species is pebble-shaped and very laterally compressed (Plate lII, 14, 17), while Gaarderia angusta (Plate lII, 2) and G. lata (Plate III, 11 ) are ovally-shaped and not laterally compressed. The sulcal membranes in Gaarderia compressa are very unevenly located (Plate III, 15) while in the latter two species they are not (Plate III, 2, 11). Due to the lateral compression in Gaarderia compressa, plate C2 is located almost entirely on the left side of the cell (Plate III, 17). In Gaarderia angusta or G. lata this plate is found on the dorsal side of the cell (Plate III, 8, 12). The zone of honey-combed pores on plate 1"" is raised in Gaarderia compressa (Plate III, 17) while it is not in G. angusta (PlatelII, 7) or in G. lata (Plate III, 11 ). In Lissodinium, which is also laterally compressed, plates 1" and 4" are the widest, whereas the dorsal plates 2" and 3" are symmetrical as well as the narrowest (Fig. 3B). In Gaarderia compressa and in G. armata, the dorsal plates 3" and 4" are asymmetrical while plates 2" and 5" are the widest in the epitheca, and plate 1" is the narrowest (Plate lII, 16; Plate IV, 1). Gaarderia

95

compressa is closely related to G. armata. The differences between these two species are summarized under Gaarderia armata.

Gaarderia armata Carbonell-Moore, sp. nov. (Plate I, 11; Plate IV, 1-5; Figs. 4H, 8M) Holotype: Plate I, 11; Plate IV, 1-5. Total length: 46.5/~m. Dorso-ventral axis: 44.9 pm. Lateral axis: 28.6 #m. SEM specimen No. 429, kept at Oregon State University, College of Oceanic and Atmospheric Sciences, Corvallis, OR, USA. Type locality: Equatorial Pacific 5°N 140°W, found between 150 and 200 m. Etymology: The appearance of the cell resembles a medieval armor. From Latin arma = armed. Diagnosis: Cellula lapilliformis et lateraliter compressa, latere ventrale acuto et latere dorsale curvato. Lamina antica intercalaris latere laevo lato; membranae sulci maginalibus serratis," zona crassissima pororum favosorum in lamina 1"'. Laminae C1 and C3 angustissimae. Formula laminarum: Po Pt X 3' la 5" 3C 4S 5" 1"'.

The pebble-shaped cells are laterally compressed, with a pointed ventral side and a curved dorsal side. The anterior intercalary plate has a wide left side, sulcal fin, serrated edges and a very thick zone of honey-combed like pores on plate 1"". Plates C1 and C 3 are very narrow. Plate formula: Po Pt X 3' la 5" 3C 4S 5"' 1"'. Description: The pebble-shaped, very laterally compressed cells have a pointed ventral side and a curved dorsal side (Plate IV, 4). They have a large apical pore complex, with a not very long ridge (Plate IV, 1). Plates 2' and 3' are short and wide (Plate I, 11; Plate IV, 1). The anterior intercalary plate has a wide left side which makes the plate very long. This plate has the shape of a truncated boomerang. Plates C1 and C3 are very narrow (Plate IV, 2) while C2 is enormous (Plate IV, 3). Plates 2" and 3" are not very narrow (Plate IV, 2, 5). Plate 4" is much larger than the other postcingulars (Plate IV, 4, 5). Both large sulcal fins have serrated edges (Plate IV, 2, 4, 5). There is a very thick and raised zone of honey-combed pores on the large plate 1"" which is visible under the light microscope (Plate IV, 4, 5). The thecal plate pores are elongated in the epitheca (Plate IV,

96

M.C. CarbonelI-Moore/Review ~[Palaeobotany and Palvnology 84 i 1994~ 73 ~)9

1, 3). Large round pores are lbund in the hypothecal plates (Plate IV, 5). The pores on the cingular plates are also round but smaller and more scattered (Plate IV, 2, 4, 5). This species is distinctively shaped and easily identifiable under the light microscope. Total length: 46.5-46.8/~m ; dorsoventral axis: 44.9--45.51Lm; lateral axis: 28.6 28.9/~m. Discussion: This species is closely related to Gaarderia compressa and the main differences between the two species may be summarized as follows: ( 1 ) Gaarderia armata has a much shorter ridge along the X platelet (Plate I, 11; Plate IV, 1 ) than Gaarderia compressa (Plate III, 16). (2) Plates 2' and 3' are shorter and wider in Gaarderia armata (Plate I, 11; Plate IV, 1 ) than in G. compressa (Plate III, 16). (3) In Gaarderia armata, the anterior intercalary plate has a wider left side than in G. compressa. Thus this plate is much larger in G. armata (Plate IV, 1 ) than in G. compressa (Plate III, 16) though with the same truncated boomerang shape. (4) Plates 2"' and 3"' are not as narrow in Gaarderia armata (Plate IV, 2, 5) as in G. compressa (Plate III, 15, 18). (5) The zone of honey-combed pores is extruded from plate 1.... in Gaarderia armata (Plate IV, 4, 5). This zone is just slightly raised in Gaarderia compressa (Plate II1, 17). Similarities of the species include comparable size of the precingular plates in both species (Plate III, 16; Plate IV, 1). These species are distinctively shaped and easily distinguishable under the light microscope from other laterally compressed Podolampadaceans like Lissodinium thanks to the large fins and to the antapicallylocated raised zone of honey-combed pores, which in Gaarderia armata will appear more prominent than in G. compressa.

H E T E R O B R A C T U M Carbonell-M oore, gen. no v. Type: Heterobractum striatum Carbonell-Moore, sp. BOY.

Diagnosis: Cellulae ovoideae cinguh) depresso aut sulco carentes, lamina posteingularis 1'" rnulto latior quam lamina 5"'. Cellulae bilateraliter et valde

asymmetricae. Formula laminarum." Po Pt X 3' l a 5 " 3 C 4 S 5 ' " 1"".

The ovoid cells are lacking a depressed cingulum or sulcus, have a postcingular plate 1" that is much wider than plate 5'" and have a pronounced bilateral cell asymmetry. Plate formula: Po Pt X 3' l a 5" 3C 4S 5'" 1"'. Etymology: The genus name refers to the different thecal plate sizes, of plates 1'" and 5'" which are of similar size in closely related Podolampadacean genera. From the Greek heter=different and bracte = laminate or plate. Discussion: In other Podolampadacean genera, e.g. Blepharocysta, Mysticella, Lissodinium, plates 1'" and 5'" are of similar size and so are plates 2'", 3'" and 4'" (Fig. 8B D,F). The postcingular plate series is remarkably assymetric in Heterobractum. Plate 1" is much narrower than 5'"; plate 4'" is much narrower than plates 2"' and 3'". Plate 5'" is the largest plate of the series, tbllowed by plates 2"' and 3'" (Fig. 8G). This genus also shows a cell asymmetry unique within the Podolampadaceans. Whereas most of the epithecal plates are positioned at the right side of the cell (Fig. 4C), in the hypotheca most plates have a left side position (Fig. 8G). In most Podolampadacean genera the same number of plates can be found on both the right and left side of the cell, e.g. Blepharocysta, or Lissodinium. One new species is described. Heterobractum striatum Carbonell-Moore, sp. nov. (Plate I, 6; Plate IV, 6 9: Figs. 4C, 6C, 8G) Holotype: Plate IV, 6 9. Total length: 35.5/~m.

Dorso-ventral axis: 27.5 t~m. Lateral axis: 25.9 pm. SEM specimen No. 338, kept at Oregon State University, College of Oceanic and Atmospheric Sciences, Corvallis, OR, USA. Type locality: Equatorial Pacific O'140°W, found between 150 and 200 m. Etymology: The name of the species indicates the characteristic "striated" thecal pore arrangement on most of the plates. From Latin stria = streak. Diagnosis: Cellula ovoidea, parvissima; complexum pori apicalis rotundum, brevis, lamina antica intercalaris parva, symmetrica, bracteae precingulares poris elongatis' et rotundatis alternantibus protectae.

M. C. Carbonell-Moore/Reviewof Palaeobotany and Palynology 84 (1994) 73 99 Bracteae cingularae angustae. Formula laminarum: Po Pt X 3' la 5" 3C 4S 5" 1"".

The ovoid cells have a minute, round apical pore complex, a small anterior intercalary plate and a precingular plate series covered with alternated elongated round pores. Narrow cingular plates. Plate formula: Po Pt X 3' la 5" 3C 4S 5" 1"". Description: The small ovoid cells are laterally slightly compressed (Plate IV, 6) and have no bilateral symmetry. There are three precingular plates on the right side of the epitheca (Fig. 4C) and two postcingulars on the right side of the hypotheca (Fig. 8G; Plate IV, 8). The round apical pore complex (Plate I, 6) has a very long ridge on the cover and canal plates. Plates 2' and 3' are wide with numerous round pores. The relatively small anterior intercalary plate is boomerangshaped and its vertex is symmetrically located on the middle of the epitheca (Plate I, 6). The relative size of the precingular plate series is not equal; plate 1" is the largest of all whereas plate 5" is the narrowest (Fig. 4C). The relative size of the plates in the narrow cingular plate series is similar (Fig. 6C). Plate C2 has five sides. The right sulcal plate has a wide anterior side (Plate IV, 6). The postcingular plate series is relatively large (Fig. 8G; Plate IV, 8). Plate 1" is much narrower than plate 5"', which is much wider anteriorly than 1' (Plate IV, 8). Both plates have large lists. Plates 2' and 3' are of similar size (Plate IV, 8). Plate 4'" is relatively narrow and its anterior sutures are of similar length (Plate IV, 7) and very short when compared to 4" plate of other Podolampadaceans (Fig. 6B-J). The well-developed antapical plate is covered with honey-combed pores (Plate IV, 8). The anterior intercalary and precingular plates are densely covered by alternating round and elongated pores (Plate I, 6; Plate IV, 6, 9). Plates C1 and C3 have densely-packed round pores (Plate IV, 6, 9), while C2 has, with exception to the areas along the edges of the plate, only a few pores (Plate IV, 7). Pores on the postcingular plate series are also round and densely-packed (Plate IV, 7-9). Several cells were found in the same locality as the holotype. Total length: 35.5-45.4/~m. Dorso-ventral axis: 27.5-33.7/tm. Lateral axis: 25.9-32.5 Ibm. Discussion: The main differences with other

97

Podolampadaceans have been mentioned in the comparison of the genus Heterobractum to other Podolampadacean genera. The striated pore arrangement of the epithecal plates is similar to that observed in species of Mysticella and Gaarderia.

5. Conclusions

(1) The plate formula of the family Podolampadaceae plate formula may be written as: Po Pt X 3' la 5" 3C 4-5S 4-5" 1"". This formula assumes that: (a) The three plates on the equatorial plane are the homologues of the three cingular plates of other Peridinioids. (b) The transitional plate "t" of other Peridinioids is fused to the anterior sulcal plate in the Podolampadaceans. (c) The five plates adjacent to the three cingular plates in the hypotheca are the homologues of the five postcingular plates found in the hypotheca of other Peridinioids. (d) The plate posterior to the postcingular plate series and the sulcus is the homologue of the single antapical plate in Diplopsalis sensu Dodge and Toriumi (1993). (2) Three defined types of APC were found in the Podolampadaceans: Type 1. There is only a small protuberance on the cover plate. Pores and ridges are present on the pore plate. This apical pore is found only in Blepharocysta Ehrenberg. Type 2. There is a small spine on the cover plate. Pores but no ridges are found on the pore plate. Lissodinium Matzenauer, emend. CarbonellMoore and Mysticella Carbonell-Moore, gen. nov. show this type of apical pore. Type 3. A long and pronounced ridge is found along the cover and the canal plates. The pore plate bears pores but no ridges. Gaarderia Carbonell-Moore, gen. nov. and Heterobractum Carbonell-Moore, gen. nov. show this kind of apical pore. The exact number of plates in Podolampas's APC has not been verified yet. (3) A broad range of cell bilateral asymmetry

98

M.('. CarbonelI-Moore/Review ql Palaeohotan3, and Pa@mdogy (~4 : 1~1941 73 99

and of cell compression results in a pronounced cell distortion in these dinoflagellates. This cell distortion in more evident in the different species of Gaarderia Carbonell-Moore, gen. nov. A unique bilateral plate asymmetry (and no cell compression) is observed in H e t e r o b r a c t u m Carbonell-

Moore, gen. nov. (4) Of all the plates series, the cingular series show the most variation in both development (narrow to very wide) and relative plate size within the series. (5) The finding of zygotic forms is evidence of a sexual life cycle in the Podolampadaceans. ( 6 ) Diplopsalis sensu Dodge and Toriumi ( 1993 ) appears to be a possible common ancestor of the Podolampadaceans.

Acknowledgements This study was made possible in part by the grant NSF-8914885 to Dr. K.A. Steidinger. 1 am very grateful to all the people who provided samples for this study: Drs. G.A. Fryxell, G.M. Hallegraef, D. Marino, M. Montresor, T.J. Smayda, P.A. Tester and T. Villareak Mr. E. Zettler kindly collected samples for me. My deepest gratitude to Ms. A. Benbow, Dr. H. Dahm and Dr. M. Roman, who made the Equatorial Pacific subsamples available. Drs. B. Sherr and E. Sherr generously allowed the use of their inverted microscope for cell isolations. Thanks to Ms. K. Amthor who translated German text and to Dr. E. Truby for his assistance with the SEM. My heartful thanks to Dr. Karen A. Steidinger whose help and support to this study are invaluable. I would like to acknowledge Dr. L.I. Gordon for his generous support. Many thanks to Prof. Enrique Balech who inspite of his work overload found the time to review this manuscript. Most of all I thank my husband Sandy for his continuous support and encouragement.

References Abe, T.H.. 1 9 6 6 . The armoured Dinoflagellata: Podolampidae. Pub1. Seto Mar. Biol. Lab., 14:129 154.

Balech, E., 1954. Sur la tabulation de Podolumpas et Oxytoxum. Rapp. Commun. 8e Cong. Int. Bot., Sect. 17:114 116. Balech, E., 1963. La familia Podolampaceae (Dinoflagellata). Bol. Inst. Biol. Mar. Mar del Plata, 2:3 27. Batech, E., 1974. El g6nero Protoperidinium Bergh, 1881 ("Peridinium" Ehrenberg, 1831, part#~s). Rev. Mus. Argent. Cienc. Nat. Bernardino Rivadavia. hast. Nac. Invest. Cienc. Nat. Hidrobiol., 4( 1 ): I 79. Balech, E., 1980. On thecal morphology of dinoflagellates with special emphasis on cingular and sulcal plates. An. Cent. Cienc. Mar, Limnol. Uni~. Nac. Auton. M6xico, 7:57 67, Balech. E., 1988. Los Dinoflagelados del Atlfintico Sudoccidental. Inst. Esp. Oceanogr., Madrid, 310 pp. Bfitschli, O., 1885. Dinoflagellata. In: H. G. Bronn (Editor), Protozoa (Mastigophora) 1t88tl 1889). Klass. Ordn. Thierreichs, 1. Winter, Leipzig, pp. 9116 1029. Carbonell-Moore, M.C.. 1991. Lissodinium Matzenauer, emend., based upon the rediscovery of L, schilleri Matz.. another member of the family Podolampadaceae Lindemann (Dinophyceae), Bot. Mar., 34:327 3411. Carbonell-Moore. M.C.. 1992. Blepharo~3,sla hermosillai, sp. no~. a new member of the family Podolampadaceae Lindemann (Dinophyceae). Bot. Mar., 35:273 281. Carbonell-Moore, M.C.. 1993. Further observations on the genus Lis,~odinium Matz,. ememl., Carbonell-Moorc (Dinophyceae), with descriptions of seventeen new species. Bot. Mar., 36:561 587 Carbonell-Moore. M.C., 1994. On the biogeography of the family Podolampadacea Lmdemann (Dinophyceae) vertical and latitudinal distribution. Rev. Palaeobot. Palynoh. 84: 23 44. this issue. Dodge, J.D. and Hermes, ll.B., 1981a. A scanning electron microscopical study of the apical pores of marine dinoflagellares (Dinophyceae). Phycologia. 20:424 430. Dodge. J.D. and Hermes. H.B.. 1981b. A revision o1 the Diplopsalis group of dinoltagellates (Dinophyceae) based on material from the British Isles. Bot. J. kinn. Soc., 83:15 26. Dodge. J.D. and Toriumi, S., 1993. A taxonomic revision o1" the Diplopsalis group (Dinophyceae). Bot. Mar.. 36:137 147. Fensome, R.A., Taylor, F.JR.. Norris, G., Sarjeant. W.A.S., Wharton, D.I. and Williams. G.L., 1993. A Classification of I,iving and Fossil Dinoflagellates. Micropaleontology, Spec. Publ.. 7, 351 pp. Gaarder, K.R,, 1954. Dmoflagellatac from the "Michael Sars'" North Atlantic Deep-Sea Expedition 1910. Rep. Sci, Res. "Michael Sars'" North-All. Deep-Sea Exped. 1910, 2(31: 1 62 pp. Gaines, G. and Elbr'achtcr, M., 1987. Heterotrophic nutrition. In: F.J.R. Taylor (Editor), The Biology of Dinoflagellates. Blackwell, Oxford, pp. 224 268. Hallegraeff, G.M. and Jeffrey, S.W., 1984. Tropical phytoplankton species and pigments on continental shelf waters of north and north-west Autralia. Mar. Ecol. Prog. Ser.. 20:59 74. Hallegraeft, G.M. and l,ucas. I.A,N, 1988. The marine dinotlagellate genus Dinophysis (Dinophyceae): photosyn-

M. C. Carbonell-Moore/Review of Palaeobotany and Palynology 84 (1994) 73 99 thetic, neritic and non-photosynthetic, oceanic species. Phycologia, 27: 25-42. Jacobson, D.M. and Anderson, D.M., 1992. Ultrastructure of the feeding apparatus and myonemal system of the heterotrophic dinoflagellate Protoperidinium spinulosum. J. Phycol., 28: 69-82. Kofoid, C.A., 1909. The morphology of the skeleton of Podolampas. Arch. Protistenk., 16: 48-61. Lewis, J., 1990. The cyst-theca relationship of Oblea rotunda (Diplopsalidaceae, Dinophyceae). Br. Phycol. J., 25: 339 351. Lewis, J., 1991. Cyst-theca relationships in Scrippsiella (Dinophyceae) and related orthoperidinioid genera. Bot. Mar., 34:91 106. MacKenzie, L., 1992. Does Dinophysis (Dinophyceae) have a sexual life cycle? J. Phycol., 28: 399-406. McKenzie, C.H., 1985. Armored Dinoflagellates of the Southwestern Atlantic Ocean. PhD Dissertation. Texas A', College Station, TX, Vols. I and II, 392 pp. Nie, D., 1939. Dinoflagellata of the Hainan region. II. On the thecal morphology of Blepharocysta, with a description of a new species. Contrib. Biol. Lab. Sci. Soc. China Zool. Ser., 13: 23-39. Nie, D., 1942. Dinoflagellata of the Hainan region. IV. On the thecal morphology of Podolampas with description of species. Sinensia, 13: 53-60.

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Pfiester, L.A. and Anderson, D.M., 1987. Dinoflagellate reproduction. In: F.J.R. Taylor (Editor), The Biology of Dinoflagellates. Blackwell, Oxford, pp. 611-648. Pfiester, L.A. and Skvarla, J.J., 1979. Heterothallism and thecal development in the sexual life history of Peridinium Volzii (Dinophyceae). Phycologia, 18:13 18. Rampi, L., 1941. Ricerche sul fitoplancton del Mare Ligure. 5. Le Podolampacee delle acque di Sanremo. Ann. Mus. Civ. Stor. Nat. Doria Genova, 61: 141-152. Schiller, J., 1937. Dinoflagellatae (Peridineae) in monographischer Behandlung. Rabenhorst's Kriptogamen-Flora, 10(3), 2(3/4): 321-590. SchOtt, F., 1895. Die Peridineen der Plankton Expedition. Ergeb. Plankton-Exped. Humboldt Siftung, 4: 1-170. SchOtt, F., 1896. Peridiniales. In: H.G.A. Engler and K. Prantl (Editors), Die naturlichen Pflanzenfamilien. Leipzig, I(lb), pp. 1-30. Steidinger, K.A. and Williams, J., 1970. Dinoftagellates. Mem. Hourglass Cruises (Florida Dep. Nat. Resour. St. Petersburg), 2: 1-251. Taylor, F.J.R., 1980. On dinoflagellate evolution. Biosystems, 13: 65-10. Taylor, F.J.R., 1987. Dinoflagellate morphology. In: F.J.R. Taylor (Editor), The Biology of Dinoflagellates. Blackwell, Oxford, pp. 24-91.