Ciliophora, Protista - Helgoland Marine Research

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Campbell ( 1929, 1939) is based solely on the morphology of the lorica. ... (1931), Candelas (1932), Gaarder (1946), Marshall (1969) and Souto (1981), usingĀ ...
HELGOL.ANDER MEERESUNTERSUCHUNGEN Helgol~nder Meeresunters. 51, 155-172 (1997)

Tintinnina (Ciliophora, Protista) of the North Sea during the spring of 1986 T. A. C o r d e i r o I & R. S a s s i 2 ICentro de Estudos do Mar, Universidade Federal do Paran~; Av. Beira M a r s/n, 83255-000 Pontal do Sul - PR, Brasil 2NEPREMAR, Universidade Federal da Parafba; C a m p u s Universit~rio, 58059-900 Jo~o Pessoa - PB, Brasil

ABSTRACT: This work is the first of a series in which the distribution patterns and the importance of the Tintinnina in the trophic chain of the North Sea are evaluated. In agreement with Foissner (1994), who stated "Most ecological papers on planktonic protozoans lack reliable identifications and modern nomenclature ...", the series will start with the results of a taxonomic revision. Illustrations and brief descriptions of the 23 Tintinnina species found in this analysis are given, as well as comments about species identification. Differences between the present results and the previous work of Lindley (1975) can indicate some changes in the species structure. A higher number of species was found than that found by Lindley (1975) in seasonal samplings.

INTRODUCTION Despite m a n y works on Tintinnina, i n c l u d i n g those on the North Sea sp eci es (e.g. Jorge ns en , 1899; Brandt, 1907; Hofker, 1931), the t a x o n o m y of the group is far from b e i n g a c c e p t e d as definite (Laval-Peuto & Brownlee, 1986). Th e system p r o p o s e d by Kofoid & C a m p b e l l ( 1929, 1939) is b a s e d solely on the m o r p h o l o g y of the lorica. H o w e v e r , w e k n o w today that variations in the s h a p e and size of the lorica occur with f r e q u e n c y d u e to changes in t e m p e r a t u r e , salinity, food c o n c e n tr a ti o n (Gold & Morales, 1975), cellular division rates (Gold, 1970; Verity, 1987; Pierce & Turner, 1992), p o l y m o r p h i s m in biological cycles (Laval-Peuto, 1981), a n d the formation of resistance spores (Kamiyama & Aizawa, 1990). Some p i o n e e r w o r k s such as D a d a y (1887), Brandt (1907), Schulz & Wulff (1929) and H o f k e r (1931) called attention to the inter-specific variations in the shape of the lorica an d followed the use of cell m o r p h o l o g y to m a k e safer descriptions an d identifications. Usually, however, f o r m a l d e h y d e and lugol are used as p r e s e r v i n g agents in m a r i n e biology, w h i c h retains only the lorica of the Tintinnina, g i v i n g a w i d e m a r g i n for the occurr e n c e of synonyms, such as those i n c l u d e d in the revisions of Kofoid & C a m p b e l l (1929,1939) an d w h i c h h a v e b e e n a d o p t e d by most of the authors w h o f o l l o w e d them. At present, the silver-protargol t e c h n i q u e is b e i n g u s e d m o r e frequently, p e r m i t t i n g comparisons of the tintinnids at the infracilliature l e v e l (Brownlee, 1977; S n y d e r & Brownlee, 1991; Choi et al., 1992); however, the n u m b e r of works is still insufficient to a t t e m p t a n e w revision b a s e d on the m o r p h o l o g y of the cell. E v e r y t h i n g indicates that the lorica morp h o l o g y shall remain, for the time being, the usual w a y to identify tintinnids. 9 Biologische Anstalt Helgoland, Hamburg

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In this context, it seems appropriate to p r e s e n t the results of a taxonomic revision of a collection from the whole North Sea, t a k e n in spring of 1986, where only the lorica morphology was considered. This work should become, in a g r e e m e n t with Foissner (1994), a basis for the discussion about the ecology of the T i n t i n n i n a in the North Sea. This revision does not solve all the problems c o n c e r n i n g the identification of T i n t i n n i n a from the North Sea, but, instead, stresses the necessity for more investigations in the future. The figures, descriptions a n d original references m a y prove to be helpful for future studies.

MATERIAL AND METHODS The major objective of the G e r m a n ZISCH p r o g r a m {acronym for "Zirkulation u n d Schadstoffumsatz in der Nordsee" - "Circulation a n d Pathways of Pollutants in the North Sea") was to actualize the existing data on the e n v i r o n m e n t a l conditions in the North Sea in relation to anthropic activity. Its fulfillment involved some research institutes of the Federal Republic of G e r m a n y a n d d e p e n d e d on the s i m u l t a n e o u s mission of three oceanographic vessels: F. S. "Valdivia", K S. "Gauss" a n d the P.S. "Planet". O n e of the particip a t i n g institutes was the Biological Station of H e l g o l a n d (Biologische Anstalt Helgoland), w h e r e the m i c r o p l a n k t o n samples of this work are deposited. The p r o g r a m was accomplished in two stages, one in spring (1986) a n d the other in winter (1987). The p r e s e n t study was m a d e u s i n g as basis 129 o c e a n o g r a p h i c stations distributed in radials from the g e o g r a p h i c a l center of the North Sea, d u r i n g the late spring, b e t w e e n M a y 2 n d a n d J u n e 3rd, 1986. A total of 265 samples from 60 stations was selected for the analysis of the Tint i n n i n a (Fig. 1). M i c r o p l a n k t o n was collected with 5-liter Niskin bottles at 5 depths per station. The s a m p l e d depths varied according to the station a n d the thermocline depths. In shallow stations, in depths less than 30 m, only 3 or 4 depths were sampled. The s a m p l e s were c o n c e n t r a t e d with a mesh of 20 lxm a n d kept in 2% formaldehyde n e u t r a l i s e d with borax. Microscopic analysis was carried out with a n inverted microscope a c c o r d i n g to the Uterm6hl (1958) technique, using s e d i m e n t a t i o n c h a m b e r s of 10, 25 a n d 50 ml. In order to permit the identification of the species level, it was necessary to p h o t o g r a p h different specim e n s with a c o m m o n reflex camera, a d a p t e d to the lens of the microscope. The identification of the T i n t i n n i n a was b a s e d principally on the works of J o r g e n s e n (1899, 1924, 1940), Brandt (1906, 1907), M e u n i e r (1919), Kofoid & C a m p b e l l (1929, 1939], Hofker (1931), C a n d e l a s (1932), G a a r d e r (1946), Marshall (1969) a n d Souto (1981), u s i n g only the lorica morphology as diagnostic criterion. The systematic position of the s u b o r d e r Tintinn i n a adopted in this work was proposed by M o n t a g n e s & Lynn (1991): PROTISTA k i n g d o m PROTOZOA s u b k i n g d o m CILIOPHORA p h y l u m SPIROTRICHEA class CHOREOTRICHIDA order TINTINNINA s u b o r d e r

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T.A. Cordeiro & R. Sassi RESULTS

Following the analysis of 265 samples of microplankton, 23 species w e r e identified, distributed in 9 families a n d 12 g e n e r a , which are h e r e b y listed as follows:

Family T i n t i n n i d i d a e Kofoid & Campbell, 1929

Leprotintinnus pellucidus (Cleve, 1899) (Fig. 2 a). Few loricae were f o u n d d u r i n g the analysis of the samples of the ZISCH program; all occurrences were from the Baltic Sea a n d the coast of Norway. A notable characteristic of this species is the o p e n lorica in the two extremities, the diameter diminishes from the oral to the aboral region, the u p p e r part is h y a l i n e a n d the presence of a d h e r e d particles increases gradually in the lower region, the aboral aperture is slightly e n l a r g e d a n d covered with particles. The m e a n ratio betw e e n l e n g t h a n d b r e a d t h is 6.3.

Family C o d o n e l l i d a e Kent, 1882

Tintinnopsis beroidea Stein, 1867 (Fig. 2 b). The lorica is cylindrical, w i d e n i n g slightly in direction of the oral aperture a n d e n d i n g in a cone whose profile r e s e m b l e s a n isosceles triangle: b e i n g totally covered by particles such as grains of sand, which give the surface a g r a n u l a t e d appearance. The l e n g t h is quite variable during the developm e n t of the cell, which gives room for the creation of m u c h synonymity. However, rarely does the l e n g t h exceed 120 pm. T. cf cylindrica Daday, 1887 (Fig. 2 c). Only one lorica of this species was f o u n d on the surface of station 97. The lorica has a g r a n u l a t e d a p p e a r a n c e as a result of the p r e s e n c e of a d h e r e d particles, is uniformly cylindrical up to the aboral cone, where a p r o n o u n c e d p e d u n c l e is located which corresponds to approximately 1/5 of total length a n d characterizes this species. T. nana Lohmann, 1908 (Fig. 2 d) occurred only at station 45. The lorica is covered with material grasped by the cell a n d has small d i m e n s i o n s (Table 1), is the s h a p e of a w e d g e with a slightly r o u n d e d profile. The oral region represents the widest part, from here on the d i a m e t e r diminishes gradually until the lorica terminates in a slightly rounded aboral end. T. parvula (Jorgensen, 1899) (Fig. 2 e). The lorica is covered by particles as are all other Tintinnopsis a n d is slightly bigger t h a n T. nana. The widest part is located n e a r the middle region, giving the lorica the a p p e a r a n c e of a sectioned ellipse, a n d the aboral region is conical. T. cf spiralis (Meunier, 1910) (Fig. 2 f). Only one lorica of this species was f o u n d at a d e p t h of 300 m at station 99, which p r e v e n t s a reliable identification. The lorica is elongated; from the oral aperture until the superior third the d i a m e t e r diminishes b y a r o u n d 1/5, i n c r e a s i n g a g a i n until the inferior third a n d henceforth d i m i n i s h i n g until t e r m i n a t i n g in a sharp angle. This s p e c i m e n differs from that described by Marshall (1969), w h i c h has spiral striation in the wall of the lorica. T. tubulosa Levander, 1900 (Fig. 2 g) was restricted to stations 45 a n d 47, h o w e v e r in densities which vary b e t w e e n 19 a n d 78 ind. 1-1. The lorica is approximately cylindrical, s h o w i n g a slight n a r r o w i n g b e n e a t h the oral aperture, with a small ratio b e t w e e n l e n g t h

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a n d diameter in relation to all other species of T i n t i n n i n a described in this work (1.8); as such, length rarely attains d o u b l e the d i a m e t e r m e a s u r e d in the oral region. Tintinnopsis sp. (Fig. 2 h) occurred in small quantities in the stations in the English C h a n n e l , in the G e r m a n Bight, a n d along the coast of Norway. As in all the other Tintinnopsis, the lorica was completely covered with particles. The broadest part is in the middle region, t a p e r i n g very little in direction of the oral aperture a n d strongly toward the base. The inferior part of the lorica resembles one half of an ellipse.

Family C o d o n e l l o p s i d a e Kofoid & Campbell, 1929

Stenosemefla nivalis (Meunier, 1910) (Fig. 3 a). This was the most a b u n d a n t species in the samples, s u p e r s e d i n g all the others in the n u m b e r of individuals s a m p l e d a n d freq u e n c y in the a n a l y s e d stations, a p p e a r i n g in more t h a n 52 % of the samples. The lorica is small a n d covered with foreign particles, the g e n u s Stenosemefla differing from Tintinnopsis in the p r e s e n c e of a n oral collar, normally hyaline a n d free of encrustations. The ratio b e t w e e n l e n g t h a n d b r e a d t h is small (1.3), the largest part b e i n g u n d e r the oral collar tapering until the base, forming an o p e n angle. Stenosemella producta (Meunier, 1919) (Fig. 3 b) occurred in only 5 samples. The morphological p a t t e r n of the lorica is similar to that of S. nivalis, h o w e v e r slightly longer a n d narrower, with a n e v i d e n t shoulder n e a r the collar. Codoneflopsis ovata J e r g e n s e n , 1924 (Fig. 3 c). Few individuals of this species were found, in depths of about 200 m at stations n ~ 115 a n d 117. Of small dimensions, the lorica is spheric a n d lightly covered by particles. The oral collar is quite fragile a n d often hard to observe. Family Coxliellidae Kofoid & Campbell, 1929

Coxliella pseudoannulata (Jergensen, 1901) (Fig. 3 d). This species occurred only at stations n e a r the N o r w e g i a n coast. The lorica is b a n d e d in a spiral formation in which the n u m b e r of rings is quite variable. The wall of the b a n d s shows an alveolar structure, which is a distinctive characteristic of the g e n u s Coxliella. The separation b e t w e e n the cylinder a n d aboral cone is well defined a n d located in a region b e t w e e n half a n d lower third of the length. Helicostomella subulata (Ehrenberg, 1833) (Fig. 3 e) is a cosmopolitan species, wellk n o w n a n d very c o m m o n in the Baltic Sea a n d the G e r m a n Bight. Being a species of large dimensions, it contributed greatly to the total biomass of Tintinnina. The lorica is cylindrical, does not have encrustations, a n d the ratio b e t w e e n l e n g t h a n d d i a m e t e r is high, a r o u n d 8. The p e d u n c l e is long a n d wide, surpassing by 1/5 the total length. The oral aperture is serrated or denticulate. Rings with the same serrated structure are observed for the whole u p p e r third of the lorica, p r o b a b l y as a result of successive depositions during its growth cycle. Family Ptychocylidae Kofoid & Campbell, 1929

Favefla ehrenbergii (Clapar6de & L a c h m a n n , 1858) (Fig. 3 f). The description of F. helgolandica g i v e n by Hofker (1931) corresponds exactly to the s p e c i m e n s f o u n d in this

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Fig. 3. C o d o n e l l o p s i d a e , Stenosemella niva]is (a), S. producta (b), Codonellopsis ovata (c); Coxliellidae, Coxliella pseudoannulata (d), Helicostomella subulata (e); Ptychocylidae, Favella ehrenbergii (f), PtychocFtis urnula (g), P. urnula [minor] [h); Petalotrichidae, Acanthostomella norvegica (i). Distances in g m

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investigation; but for reasons which will be e x p l a i n e d hereafter, the n a m e F. ehrenbergii was retained. The lorica is larger t h a n that of the other species (Table 1), the shape is cylindrical with a ratio b e t w e e n length a n d d i a m e t e r of 2.7. A slight constriction occurs in the oral aperture, together with a variable n u m b e r of rings, which are s u p e r i m p o s e d during growth. The aboral cone is round, starting approximately from a third of the length a n d t e r m i n a t i n g in a p e d u n c l e which in g e n e r a l attains 1/7 of the total length. The wails of the lorica are thick b u t hyaline, without particle a c c u m u l a t i o n but of a coarse texture. Favella sp. (not illustrated). Only one s p e c i m e n found; the lorica was covered with an u n k n o w n material, possibly oil, which m a d e the identification to species level impossible. Ptychocylis urnula (Clapar6de & L a c h m a n n , 1858) (Fig. 3 g-h). P. urnula was widely distributed t h r o u g h o u t the North Sea, c o n t r i b u t i n g largely to the total biomass of the Tintinnina. The lorica is identified by its cylindrical shape, with a small e n l a r g e m e n t u n d e r the oral aperture a n d by the conical shape in the aboral region which t e r m i n a t e s with a short peduncle, tn vertical section, the cone ridge forms a n a n g l e of a p p r o x i m a t e l y 45 ~ with the cylinder wall. The edge of the oral aperture is serrated a n d the sides of the whole lorica show a certain rugose texture. The proportion b e t w e e n the l e n g t h a n d diameter is approximately 1.8.

Family Petalotrichidae Kofoict & Campbell, 1929

Acanthostomella norvegica (Daday, 1887) (Fig. 3 i). Species of small d i m e n s i o n s a n d very a b u n d a n t along the N o r w e g i a n coast. The lorica is quite fragile a n d difficult to observe, the refraction of the lorica walls is very close to that of water. The inferior region is h e m i s p h e r i c with a smalI, aborat p e d u n c l e . The u p p e r half forms a cylinder with a height approximately e q u i v a l e n t to half the total length. The oral aperture is d e n t i c u l a t e on the m a r g i n s a n d with a narrow flank u n d e r n e a t h which encircles the oral o p e n i n g . Family Xystonellidae Kofoid & Campbell, 1929

Parafavella denticulata (Ehrenberg, 1840) (Fig. 4 a) is the second largest species f o u n d in the ZISCH program. Small quantities occurred at 15 stations, the species was a b s e n t in the English C h a n n e l a n d the G e r m a n Bight. The lorica is cylindrical a n d the walls show a typical p a t t e r n for this genus, similar to the h o n e y c o m b s of a beehive. The oral a p e r t u r e is d e n t i c u l a t e d a n d the base of the lorica t e r m i n a t e s in a p e d u n c l e which attains approximately 1/7 of total length. The l e n g t h of the lorica is quite variable, despite the fact that the d i a m e t e r of the oral region could be considered constant (Table 1), the l e n g t h - d i a m e t e r ratio varied from 2.4 to 4.8. R elegans (Ostenfeld, 1899) (Fig. 4 b-f) showed the largest biomass on the west coast of Norway, b e c o m i n g the d o m i n a n t species in the region. The s h a p e of the lorica is slightly variable b u t always keeps cylindrical-conical. The wall of the lorica shows hexag o n a l alveoli, a n d the oral aperture presents, in the most cases, denticles curving outwards. The p e d u n c l e is generally long a n d fine, a t t a i n i n g up to 1/3 of the total length. The m e a n ratio b e t w e e n total l e n g t h a n d d i a m e t e r is a r o u n d 3.4. P. parumdentata (Brandt, 1906) (Fig. 4 g-h). Identification was b a s e d o n the descriptions by Marshall (1969). The lorica is conical as in P. elegans, but of smaller proportions;

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the walls show a h o n e y c o m b - l i k e texture, as in all the other Parafavella. T h e p e d u n c l e is very short or a b s e n t a n d the m a r g i n of the oral a p e r t u r e is serrated. Parundella caudata (Ostenfeld, 1899) (Fig. 5 a). Few loricae of this species h a v e b e e n found, which up to the p r e s e n t time does not pose difficulties as to its taxonomy. P. caudata was found only in the Baltic Sea a n d on the coast of Norway, at stations 99, 101,105 a n d 115. The lorica is totally hyaline, with thick walls, without the p r e s e n c e of foreign material or striae, alveolus, etc. The shape of the lorica is that of a n e l o n g a t e d cone, slightly curved, with a slight n a r r o w i n g where the aboral p e d u n c l e starts, w h i c h attains approximately 1/5 of the total length.

Family T i n t i n n i d a e (Claparede & Lachmann, 1858)

Salpingefla acuminata (Clapar&de & L a c h m a n n , 1858) (Fig.5 b-d) was p r e s e n t in neritic a n d oceanic areas in the n o r t h e r n half of the studied area, t h o u g h not occurring in the Baltic Sea. The lorica is fine a n d hyaline, the oral aperture is dilated like that of a trumpet, b e i n g able to attain double the b r e a d t h of the lorica. The aboral c o n e is coiled as in Salpingacantha undata a n d the ratio b e t w e e n the length a n d d i a m e t e r is 15.5. Salpingacantha undata (Jorgensen, 1899) (Fig. 5 e-f). Few loricae of this species were found, and were identified on the basis of the descriptions by J o r g e n s e n (1899) a n d Marshall (1969). This species was also p r e s e n t only in the northern part of the s t u d i e d area, m a i n l y n e a r the coasts of Scotland a n d Norway. The lorica is long a n d h y a l i n e , with the aboral region g e n e r a l l y b e i n g coiled to the right forming grooves in a spiral p a t t e r n . The oral m a r g i n is w i d e n e d a n d d e n t i c u l a t e d in v a r y i n g shapes a n d quantities. T h e l e n g t h of the lorica attains on average 14 times its breadth. The m e a n values of length, d i a m e t e r a n d v o l u m e of the lorica of each i d e n t i f i e d species, as well as the n u m b e r of m e a s u r e d individuals, are shown in Table 1.

DISCUSSION The greatest difficulty in the identification of the material from the Z I S C H p r o g r a m was due to the g e n u s Tintinnopsis. Baker & Phaff (1976) considered T. beroidea, T. minuta, T. nana, T. parvuta a n d T. rapa variations of the same species. In the p r e s e n t work, T. parvula, T. nana a n d T. beroidea showed different shapes a n d sizes, a n d for this reason were considered separately in the e v a l u a t i o n of the biomass. Nevertheless, this does not invalidate the suppositions of Baker a n d Phaff, if we consider the degree of polymorp h i s m already s e e n in the other genera, such as Favefla (Laval-Peuto,1981), Ptychocylis (Schulz & Wulff, 1929; Davis, 1981) a n d Cymatocylis (Wasik & Mikolajczyk, 1994). Some loricae f o u n d r e s e m b l e d those of T. rapa, which were attributed to T. parvula, since the v o l u m e of the lorica a n d the geographic distribution were similar. O u r T. beroidea was similar to T. karajacensis Brandt (1906), which could be another s y n o n y m of this very polymorphic species. T. beroidea is one of the cosmopolitan species w i d e l y distrib u t e d both in tropical a n d temperate neritic waters of the world. T. tubulosa from ZISCH Program r e s e m b l e s also some s p e c i m e n s of T. lata Meunier, which were i l l u s t r a t e d b y Balech (1945).

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Table 1. M e a n lorica d i m e n s i o n s a n d v o l u m e of the Tintinnina of ZISCH p r o g r a m Species

Dimension

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Standard deviation

n (ind.)

Lorica v o l u m e (l~m~)

Leprotintinn us peHucidus

diameter length diameter length diameter length diameter length diameter length diameter length oral diam, diameter length diameter length diameter length oral diam. diameter length oral diam. diameter length oral diam. diameter length diameter length diameter length diameter length diameter length diameter length diameter length diameter length diameter length diameter length diameter length diameter length

38 244 35 86 40 154 25 63 27 50 29 91 36 43 78 31 53 40 54 25 39 66 23 30 40 19 48 106 24 185 86 234 91 194 85 151 29 42 57 197 50 168 49 115 42 121 18 279 18 256

2 62 4 17

11 10 64 64 1 1 2 2 64 65 1 1 1 7 7 10 10 107 106 66 6 6 5 2 2 2 7 7 73 73 8 8 1 1 58 57 36 37 12 12 26 26 15 15 6 6 26 26 11 11

276.271

Tintinnopsis beroidea T. cf cylindrica

T, nana T parvula T cf spiralis

T tubulosa Tintinnopsis sp. Stenosemella nivalis

S. producta

Codonellopsis ova ta

Coxliella pseudoannulata Helicostomella subulata Favella ehrenbergii Favella sp. Ptychocylis urn ula Acanthostomella norvegica Parafavella denticulata P. elegans lq parumdentata Parundella caudata Salpingella acuminata Salpingacantha undata

5 1 2 6

2 6 9 13 3 4 2 5 5 6 3 8 4 5 10 1 40 4 17

6 9 2 5 6 73 4 26 2 15 1 5 2 27 1 22

71.611 154.818 24,554 15.293 53.661

99.216 26.841 43.256

50.964

18.850

110.050 59.931 904.227 740.230 641.826 23.291 783.007 634.512 157.585 65.469 59.879 55.483

166

T.A. Cordeiro & R. Sassi

The aboral region of our T. cf cylindrica is more regularly conical t h a n the typical T. cylindnca, r e s e m b l i n g also T kofoidi Hada, 1938 a n d T. aperta Brandt, 1906, two very close species which seem to be highly polymorphic: Some loricae of T. aperta were pictured with a more p r o m i n e n t projection n e a r the middle region, r e s e m b l i n g some T. tocantinensis specimens. We have m a i n t a i n e d our s p e c i m e n s as T. cf cyiindHca b u t we believe it is very u r g e n t to m a k e a revision of the cylindrica-kofoidi-aperta-tocantinensis complex, which m a y b e different m o r p h o t y p e s of the same species. The species Codonellopsis ovata, first described by J e r g e n s e n (1899) as a variety of Codonella lagenula {Codonella lagenula var ova ta J e r g e n s e n , 1899), was raised to the status of species by Kofoid & C a m p b e l l (1929) who accepted as the type locality the Berg e n Coast, Norway. It seems to be a rare species in the m a r i n e plankton. O t h e r registers include some t e m p e r a t e a n d cold waters from the Gulf of California (Osdrio-Tafall, 1941; L6pez-Ochoterena & Roure-Cane, 1970), Angola (Silva, 1954) a n d South S h e t l a n d and O r k n e y Islands (Wasik & Mikolajczyk, 1990). The characters which distinguish this species from C. contracta Kofoid & Campbell, 1929, seem to be too subjective to support the division b e t w e e n these two taxa. The specimens of H. subulata were f o u n d with a very constant oral d i a m e t e r but with highly variable total lengths (Table 1). Cospers (1972) suggests that the e x t r e m e l y variable size of H. subulata is related to temperature. The species Codonella nucula was described first by Fol (1884) a n d t h e n transferred to the g e n u s Tintinnopsis by L a a c k m a n n (1908). J o r g e n s e n (1924} created the g e n u s Stenosemmella in order to separate those Tintinnopsis which h a d a firmer lorica a n d a small oral collar; as such, the species that Fol (1884) had described b e g a n to be k n o w n as StenosemelIa nucula. In the revision m a d e by Kofoid & C a m p b e l l (1929), S. nucula was rightly placed with the s y n o n y m S. nivafis described by M e u n i e r I1910). However, Kofoid & C a m p b e l l (1929) adopted the more recent n a m e nivalis, which can be f o u n d in most publications that followed. Hofker (1931) redescribed this species a n d a d o p t e d the n a m e S. nucula, but it r e m a i n s d u b i o u s w h e t h e r the original C. nucula of Fol is a Stenosemella, since the oral collar is a b s e n t in his picture. Thus, C. nucula could be in fact a still valid Tintinnopsis species, a n d for this reason we use the n a m e S. nivalis as a d o p t e d by Kofoid & C a m p b e l l (1929). Loricae with the characteristics of S. oliva M e u n i e r (1910) were included in S. nucula. Loricae of the g e n u s Acanthostomella were found c o r r e s p o n d i n g to those of A. norvegica a n d A. gracilis, but also i n t e r m e d i a r y forms were found. All the p h e n o t y p e s of Acanthostomella were i n c l u d e d in the taxon A. norvegica, in a g r e e m e n t with Balech (1971), who described the variations in the lorica of this species. This species is widely distributed in the cold waters of the Atlantic a n d Pacific O c e a n s (Hada, 1938) a n d is considered by Davis (1985) as a holarctic species. Some loricae of the g e n u s Parafavella were found w h i c h h a d the same shape as the loricae of R edentata, which were i n c l u d e d in R elegans. The shape a n d the size of the lorica of both p h e n o t y p e s are very similar a n d the diagnostic characteristic w h i c h would differentiate them would be the a b s e n c e of a serrated c r o w n c i r c u m f e r e n c i n g the oral aperture of the lorica in R edentata. In the reference material, some loricae of R etegans were f o u n d with part of the serrated c r o w n loose. Lindley (1975) also m e n t i o n e d the phenotype P. edentata, but i n c l u d e d it in R denticulata. Perhaps the a b s e n c e of the serrated

T i n t i n n i n a of the North Sea

167

crown in P. elegans is part of the process of cellular division or lorica a u g m e n t a t i o n , where the cell withdraws the crown in order to i n c l u d e another piece, before secreting a n e w crown. If Parafavella elegans shows a complex biological cycle, alternating the shape a n d size of the lorica, as observed in the closely related g e n u s Favella (Laval-Peuto, 1981), could leave to supposition the taxon P. parumdentata, which also occurred at the stations with P. elegans, which is a morphotype of the latter. A few m i n u t e s after the cellular division the proter (or the trophont) starts the construction of a n e w lorica which resembles the shape of a n adult, but it is smaller. While the variation in the lorica of R elegans was observed (Fig. 4 b-f), it was also noted that the smaller specimens had a s h a p e resembling P. parumdentata (Fig. 4 g-h), with a short p e d u n c l e in comparison with the larger specimens. E serrata (M6bius, 1887) a n d E helgolandica (Brandt, 1906) are accepted here as syn o n y m s of E ehrenbergii. This decision was t a k e n in a g r e e m e n t with Sassi & Melo (1989), who i n c l u d e d different p h e n o t y p e s in E ehrenbergii. The specimens found d u r i n g the samplings of the ZISCH program showed a p h e n o t y p e closer to E serrata as illustrated by Marshall (1969) a n d E helgolandica m e n t i o n e d by Hofker ( 1931 ), without the p r e s e n c e of lamellas b e t w e e n the base of the lorica a n d the p e d u n c l e as in E ehrenbergii of Brandt (1906). The n a m e was defined according to priority: Tintinnus ehrenbergii Clapar~de & Lachmann, 1858, Cyttarocylis serrata M6bius, 1887 and C. helgolandica Brandt, 1906. The g e n u s Favella is due to J o r g e n s e n (1924). Laval-Peuto (1981) recognized Coxliella annulata a n d C. decipiens as polymorphic phases of E ehrenbergii. This put in doubt the validity of the whole g e n u s Coxliella and, consequently, all the family Coxliellidae. I n a s m u c h as C. pseudoannulata could also be a polymorphic p h a s e of another species, in the p r e s e n t work this n o m e n c l a t u r e was m a i n tained, since the found loricae did not correspond to the size a n d shape of the descriptions of C. annulata or of C. decipiens. The lorica with a denticulate oral aperture differentiates the g e n u s Salpingacantha from Salpingella. However, if we i m a g i n e that Salpingacantha undata could retract the m a r g i n s of the lorica a n d in so doing close the oral aperture, the result w o u l d be a n oral aperture with thorn-like u n d u l a t i o n s as in Salpingella acuminata. Speculations aside, the fact r e m a i n s that, excepting the thorn-like u n d u l a t i o n s , the loricae are extremely similar (Figs 5 b-d, 5 e-f), a n d besides this, the salinity, temperature, depth and s i g m a - T w h e r e the two species occurred are practically e q u a l (Cordeiro et al., 1997). Salpingacantha undata a n d SalpingeBa acuminata may be different n a m e s of the same species. The identification of Tintinnopsis cf spiralis was made with one unique specimen whose size and shape corresponded to the shape described by Marshall (1969), except for the absence of spiral striae. The presence or absence of striae is a taxonomical characteristic of dubious validity, since it is sometimes conditional to the availability of food (Capriulo et al., 1986). According to Marshall (1969), T. spiralis is restricted to the Arctic. However, the specimen was found at a depth of 300 m, at the entrance of the Baltic Sea at temperatures below 4 ~ The shape shown in Figure 2 f could again be a specimen of T. parvula in cellular division, especially if we observe the illustrations of other species in division made by Hofker (1931): Tintinnopsis beroidea (p. 336, Fig. 17), Stenosemella ventncosa (p. 360, Fig. 36), Codonellopsis morchella (p. 366, Fig. 45). Given the impossibility to clarify this doubt and, for motives of biomass calculations, we preferred to accept the taxon T. cf spiralis.

168

T.A. Cordeiro & R. Sassi

42

2O

9

19

18

19

i

i

12

}

i

i

i

i!

{

i: k

"

I

/ 123

',~.~'~t

312

i

'

i:;

l ~ !)

,

,

.~

276

~0

~

~

~

~9 ,,~,

i i~! 194

276

~'~ '! ~i

I

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b

C

Fig. 5. Xystonellidae, Parundella caudata (a); Tintinnidae, Salpingella acuminata (b-d), Salpingacantha undata (e-f). Distances in pm

The above-listed species, excepting T. cf spiraIis, have already b e e n r e g i s t e r e d in the North a n d Baltic seas a n d a d j a c e n t regions. Lindley (1975) showed more recent data on seasonal a n d spatial d i s t r i b u t i o n of Tint i n n i n a in the North Sea, u s i n g material available from continuous p l a n k t o n recorders (Hardy, 1941) towed by commercial ships d u r i n g the year 1965. A c o m p a r i s o n b e t w e e n the species found by Lindley a n d those of the p r e s e n t study was r e n d e r e d difficult d u e to ideritification problems. But if we consider Favella serrata as s y n o n y m of F. ehrenbergii, S t e n o s e m e l l a spp. as b e i n g various n a m e s of S. nucuJa, a n d Tintinnopsis spp. as b e i n g species of Tintinnopsis identified in the ZISCH program, we would have at l e a s t 6 of the species found by Lindley (op. cit.) in the North Sea that were not i d e n t i f i e d d u r i n g the

Tintinnina of the North Sea

169

Table 2. Species of Tintinnina found by Lindley (1975) in the North Sea, and a possible synonymity with the species found during the ZISCH program Species found by Lindley (1975)

Species from ZISCH program

AcanthostomelIa norvegica Dictyocysta elegans Codone]lopsis lagenula Eutintinnus lususundae Parundella caudata ParafaveIla denticulata PtychocyIis obtusa R urnuIa Pavella serrata HelicostomelIa subulata Parafavella gigantea group Stenosemella spp. Tintinnidium in ucicola Tintinnopsis spp. CoxlieHa pse u d o a n n ula ta

= not found not found not found

= = R urn uIa = I~ ehrenbergii = R denticulata = not found =

=

Cymatocylis spp. Epiplocylis acuminata Salpingella acuminata

not found not found

=

ZISCH program. Th e 18 taxa found by Lindley are s h o w n in Table 2, w h e r e possible synonymity with the species of the Z I S C H p r o g r a m is also shown. Th e difference in the n u m b e r of species found by Lindley and in the ZI S CH p r o g r a m is due, in part, to the m e th o d s e m p l o y e d : a) Lindley carried out seasonal sampling; b) the Tintinnina are partially r e t a i n e d by the continuous sampler, w h i ch acco r d i n g to Zeitzschel (1966), retains only 3 % of the l a r g e species such as P. gigantea and b esi d es this, c) the continuous s a m p l e r collects at a relatively constant d ep t h of 10 m and at a s p e e d superior to 10 knots. On the other hand, the d i s a g r e e i n g results could be indicating an alteration in the local population, similar to that o b s e r v e d by H a g m e i e r (1978), H a g m e i e r & B a u e r f e i n d (1990) and Rick (1990) in the case of p h y t o p l a n k t o n populations. T h e s e authors p o i n t ed out the growth of n o n - i n d i g e n o u s species, eutrophication processes an d the i n c r e a s e in h e a v y - m e t a l concentrations, respectively, as factors affecting the phytop l a n k t o n p o p u l a t i o n structure. CONCLUSIONS A total of 23 species of Tintinnina w a s identified in the North Sea during the spring of 1986. H o w e v e r , future investigations on the t a x o n o m y of the group could alter this number. S o m e doubts r e m a i n as to the validity of the taxa Tintinnopsis beroidea, T. parvula, T. nana, Parafavella parundentata, Coxliella pseudoannulata an d as to the correct ta xo n o m i c position of Tintinnopsis sp.

Salpingacantha undata and Salpingella a c u m m a t a s e e m to be different n a m e s for one an d the s a m e species. This is also the case of P. urnula and R parumdentata.

170

T . A . C o r d e i r o & R. S a s s i

T. beroidea a n d T Iaarvula w e r e r e l a t i v e l y c o m m o n in c o a s t a l r e g i o n s a n d c o u l d b e i m p o r t a n t in t h e t r o p h i c c h a i n , w h i c h i n c r e a s e s t h e n e c e s s i t y for n e w t a x o n o m i c r e s e a r c h . T h e r e w e r e d i f f e r e n c e s b e t w e e n t h e r e s u l t s o b t a i n e d p r e v i o u s l y b y L i n d l e y (1975) a n d t h o s e of t h e Z I S C H p r o g r a m , w h i c h s h o u l d b e i n v e s t i g a t e d f u r t h e r to d e t e r m i n e w h e t h e r t h e s e d i f f e r e n c e s are d u e to m e t h o d o l o g i c a l d i f f e r e n c e s or to a n a l t e r a t i o n in t h e s p e c i e s c o m p o s i t i o n of t h e T i n t i n n i n a i n t h e N o r t h Sea, like t h a t o b s e r v e d i n t h e p h y t o plankton. T h e r e e x i s t s a c o n s e n s u s b e t w e e n t h e p r e s e n t s p e c i a l i s t s t h a t t h e t a x o n o m y of t h e T i n t i n n i n a , c o n s i d e r e d t h e b e s t k n o w n a m o n g s t t h e ciliates, is in u r g e n t n e e d of r e v i s i o n . T h e v a r i a b i l i t y of s h a p e s w i t h i n a s i n g l e s p e c i e s is v e r y l a r g e a n d c o u l d l e a d t o e r r o n e o u s i d e n t i f i c a t i o n s . T h i s r e v i s i o n s h o u l d b e p e r f o r m e d w i t h m o r e c o m p r e h e n s i v e m e t h o d s , including ecology, cellular morphology, laboratory cultivations versus field s a m p l e s and c o m p a r i s o n s at t h e m o l e c u l a r level.

Acknowledffements. Gratitude is due to Dr. Peter Martens, who supplied the material from the ZISCH program for the purpose of this study, as well as to Dr. Gotram Uhlig, at that time Director of the Biological Station of Helgoland, for logistic support in the analysis of the material, and to Drs Erik Hagmeier and Frederico Brandini for literature and suggestions concerning the text. Special thanks to the anonymous referees for the suggestions regarding the text. This work was financed by the German DAAD and by the Brazilian CAPES. LITERATURE C I T E D Baker, C. & Phaff, W. J., 1976. Tintinnida from coastal waters of the S.W. Netherlands. I. The genus Tintinnolosis Stein. - Hydrobiologia 50, 101-111. Balech, E., 1945. Tintinnoinea de Quequ~n. - Physis, 20 (55), 1-15. Balech, E., 1971. Microplancton de la campafia oceanografica Productividad III.- Revta Mus. argent. Cienc. nat. Bernadino Rivadavia (Hidrobiol.) 3 (I), 1-282. Brandt, K., 1906. Die Tintinnodeen der Plankton-Expedition. Tafelerklgirungen. - Ergebn. Plankt.Exped. Humboldt-Stiff. 3 La, 1-33. Brandt, K., 1907. Die Tintinnodeen der Plankton-Expedition. Systematischer Teil.- Ergebn. Plankt.Exped. Humboldt-Stiff. 3 La, 1-499. Brownlee, D. C., 1977. The significance of cytological characteristics as revealed by protargol silverstaining in evaluating the systematics of the suborder Tintinnina. M. S. thesis, Dept. Zool., Univ. of Maryland, 146 pp Campbell, A. S., 1942. The oceanic Tintinnoinea of the plankton gathered during the last cruise of the Carnegie. - Publs. Carnegie Instn 537, 1-163. Candelas, A., 1932. Nota sobre algumas especies de Tintinnoinea da costa norte de Portugal. - Anais Fac. Ci6nc. Porto 17, 163-175. Capriulo, G. M., Taveras, J. & Gold, K., 1986. Ciliate feeding: effect of food p r e s e n c e or a b s e n c e on occurrence of striae in tintinnids. - Mar. Ecol. Prog. Ser. 30,145-158. Choi, J. Ki, Coats, D. W., Brownlee, D. C. & Small, E. B., 1992. Morphology and infraciliature of three species of Eutintinnus (Ciliophora; Tintinnina) with guidelines for interpreting Protargol-stained tintinnine ciliates. - J. Protozool. 39, 80-92. Cordeiro, T. A., Brandini, F. P. & Martens, P., 1997. Spatial distribution of the Tintinnina (Ciliophora, Protista) in the North Sea, Spring of 1986. - J. Plankt. Res. (in press.) Cospers, T. C., 1972. The identification of tintinnids (Protozoa: Ciliata: Tintinnida) of the St. A n d r e w Bay System, F l o r i d a . - Bull. mar. Sci. 22, 391-418. Daday, E. von, 1887. Monographie der Familie der Tintinnodeen. - Mitt. zool. Stn N e a p e l 7, 473-591. Davis, C. C., 1981. Variations of lorica shape in the genus Iatychocylis in relation to species identific a t i o n s . - J. Plankt. Res. 3, 81-91. Davis, C. C., 1985. Acanthostomella norvegica (Daday) in insular Newfoundland waters, Canada (Protozoa: Tintinnina). - I n t . Revue ges. Hydrobiol. 70, 21-26.

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