Abundance and species composition of Tintinnina (ciliophora) in Bahía Blanca estuary, Argentina

Estuarine, Coastal and Shelf Science (1992) 34, 295-303

A b u n d a n c e and Species C o m p o s i t i o n of Tintinnina (Ciliophora) in Bahia Blanca Estuary, Argentina a

M. S. B a r r i a de C a o Instituto Argentino de Oceanografia ( I.A.D.O.) , Avda.Alem 53, 8000-Bahia Blanca, Argentina Received 30 August 1990 and in revisedform 1 July 1991

Keywords: Ciliata; Tintinnina; numerical abundance; seasonal distribution; estuary; Argentina Coast Numerical abundance and seasonal cycle of tintinnines species were studied in the inner part of the Bahia Blanca estuary. Sampling was carried out at two fixed stations at approximately weekly intervals over the period March 1986-February 1987. Nineteen species representing five genera were recorded. Most species belonged to the genus Tintinnopsis. Maximal abundances of tintinnines, 10.1 x 1031-' and 11"3 x 1031-~ at each station respectively, were found in summer. Minimal abundances, 0-5 x 1031- ' and 0-7 x 1031- ' at each station respectively, were found in winter. Tintinnidium balechi, Tintinnopsis parva and Tintinnopsis glans were present throughout the year. Tintinnopsis gracilis, Tintinnopsis baltica and Tintinnopsis beroidea exhibited seasonal occurrence, the remaining species did not show a clear pattern of distribution. The presence of Favella taraikaensis demonstrated occasional intrusions of typical fauna of the outer estuary.

Introduction T i n t i n n i n a ( C i l i o p h o r a ) are an i m p o r t a n t c o m p o n e n t o f t h e m i c r o - z o o p l a n k t o n c o m m u n i t y . Since t h e i r identification has b e e n b a s e d u n t i l n o w exclusively u p o n m o r p h o logical c h a r a c t e r i s t i c s o f easily p r e s e r v a b l e loricae an extensive l i t e r a t u r e o n t a x o n o m y is available, w h e r e a s q u a n t i t a t i v e d a t a are scarce. Vitiello (1964), K o n o v a l o v a a n d R o g a c h e n k o (1974), H e d i n (1975), R a s s o u l z a d e g a n (1979), H a r g r a v e s (1981), P a r a n j a p e (1980, 1987), Kr~ini6 (1987a,b), S a n d e r s (1987) a n d V e r i t y (1987) have p r o v i d e d q u a n t i t a t i v e i n f o r m a t i o n o n the a b u n d a n c e a n d d i s t r i b u t i o n o f T i n t i n n i n a f r o m coastal e n v i r o n m e n t s . Balech (1945, 1948, 1951, 1964) S o u t o (1970, 1973, 1974a,b) a n d B a r r i a de C a o (1981, 1986) d e s c r i b e d t i n t i n n i n e s f r o m A r g e n t i n a ' s coastal waters b u t q u a n t i t a t i v e d a t a has n o t b e e n r e p o r t e d f r o m this area. T h e p r e s e n t s t u d y is a c o n t r i b u t i o n to t h e k n o w l e d g e o f t h e ecology o f t i n t i n n i n e s in the Bahia Blanca estuary. N u m e r i c a l a b u n d a n c e a n d seasonal changes in t i n t i n n i n e s n u m b e r s are d e s c r i b e d o v e r a p e r i o d o f 12 m o n t h s in the i n n e r p a r t o f Bahia B l a n c a estuary. °Contribution 251, Instituto Argentino de Oceanografia. 0272-7714/92/030295 + 09 $03.00/0

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Figure 1. Map showing the sampling stations in Bahia Blanca estuary. Methods Bahia Blanca estuary, which can be divided into an inner and an outer part has been described in previous papers (Barria de Cao, 1981, 1986). Samples at approximately weekly intervals were collected from two stations, Ingeniero White Port and Cuatreros Port, located in the inner part of the estuary (Figure 1). Water was collected from the subsurface (0.5 m) using a 31 Van-Dorn bottle. Samples were preserved with Lugol's iodine. Salinity and surface temperature of seawater were measured throughout the sampling period. In the laboratory, the enumeration oftintinnines was made after settling 50 ml subsamples in chambers using a Wild M 20 inverted microscope. T h e entire bottom chamber was scanned for each subsample. A total of 90 subsamples were counted, 45 from the White station collection and 45 from the Cuatreros station collection. Counts of subsamples were duplicated and averaged on ten occasions for the White station and on 12 occasions for the Cuatreros station. T h e data are shown in Table 1. Results Annual minimum surface temperatures during the sampling period were 8 °C at both stations in winter and the maximum were 24 °C at White and 24.2 °C at Cuatreros in summer. Seasonal trends in salinity also were similar at both stations. A minimum surface

Abundance and species composition of Tintinnina

297

TABLE 1. Counts of tintinnines (numbers of individuals 1 t) from duplicate samples taken on ten occasions at White station and on twelve occasions at Cuatreros station Station

Sample date

Count 1

Count 2

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4 Apr. 1986 6 July 1986 19 July 1986 1 Aug. 1986 16 Sep. 1986 10 Dec. 1986 16 Dec. 1986 10 Feb. 1987 17 Feb. 1987 24 Feb. 1987

5100 740 960 500 4900 1930 2600 3750 10080 2410

4980 700 920 580 5300 1990 2560 3570 10200 2630

5040 720 940 540 5100 1960 2580 3660 10140 2520

84.8 28.3 28.3 56"6 282.8 42.4 28.3 127-3 84.8 155-6

Cuatreros

4 Apr. 1986 6 July 1986 19 July 1986 1 Aug. 1986 16 Sep. 1986 14 Oct. 1986 21 Oct. 1986 10 Dec. 1986 16 Dec. 1986 10 Feb. 1987 17 Feb. 1987 24 Dec. 1987

5980 660 900 740 5060 1685 2670 2160 2680 3910 11210 2400

6060 700 1020 660 5220 1875 2570 2280 2800 3850 11350 2200

6020 680 960 700 5140 1780 2620 2220 2740 3880 11280 2300

56-6 28.3 84.8 56.6 113.1 134.3 70.7 84.8 84.8 42.4 99.0 141.4

salinity value of 31.4%0 was recorded at the W h i t e Station in s p r i n g a n d a value of 25.9%o at C u a t r e r o s in the fall. I n s u m m e r the water was highly saline, a t t a i n i n g m a x i m a of 40.9 a n d 41-0%o at W h i t e a n d C u a t r e r o s stations respectively. D u r i n g the s u m m e r the i n n e r part of the estuary is i n f l u e n c e d by high t e m p e r a t u r e s , lack of rain a n d c o n s e q u e n t l y evaporation. Seasonal variation in surface t e m p e r a t u r e a n d salinity are s h o w n in [ F i g u r e 2(a),(b)]. A total of 19 species of t i n t i n n i n e s b e l o n g i n g to five genera were identified ( T a b l e 2). A b u n d a n c e a n d seasonal variation of total t i n t i n n i n e s in Bahia Blanca estuary are s h o w n in F i g u r e 3. Species c o m p o s i t i o n a n d the p a t t e r n of variation were similar in both stations. A n n u a l m e a n a b u n d a n c e of t i n t i n n i n e s recorded was 2"3 x 1031-1 at W h i t e station a n d 2.5 x 1031-1 at Cuatreros. M a x i m u m a b u n d a n c e s were f o u n d in s u m m e r with peaks of 10.1 x 1031 - i at W h i t e station a n d 11-3 x 1031-1 at Cuatreros. Peaks in a b u n d a n c e also o c c u r r e d in early fall, with 5 x 1031- i at W h i t e station a n d 6 x 1031- ~at Cuatreros, a n d in late w i n t e r early s p r i n g with 5.1 x 1031-1 at b o t h stations. M i n i m u m a b u n d a n c e s of 0-5 x 1031 - I at W h i t e station a n d 0.7 x 1031-1 at Cuatreros were recorded in winter. N i n e species c o m p r i s e d 94"6 % of the total n u m b e r of t i n t i n n i n e s . T h e s e species can be g r o u p e d in a d o m i n a n t species group. A second g r o u p is f o r m e d by those species of m i n o r i m p o r t ance w h i c h were less f r e q u e n t a n d n e v e r reached high n u m b e r s . A n o t h e r g r o u p is f o r m e d b y typical species of the o u t e r part of the estuary which are recorded occasionally in the i n n e r part. Tintinnidium balechi. T h i s species described previously from this estuary b y Barria de Cao (1981) was p r e s e n t t h r o u g h o u t the year with an a n n u a l m e a n a b u n d a n c e of 489 1-1 at W h i t e station a n d 600 1-1 at Cuatreros ( T a b l e 2). I t was the m o s t a b u n d a n t species i n the s t u d y area a n d d o m i n a t e d the c o m m u n i t y , c o n t r i b u t i n g heavily to the total n u m b e r d u r i n g the s p r i n g a n d s u m m e r peaks. D u r i n g the s u m m e r peak in a b u n d a n c e it reached a m a x i m u m n u m e r of 4-9 x 1031-i at W h i t e station a n d 5.4 x 1031-1 at Cuatreros. T h i s species

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period in the investigated areas: (a) White station, (b) Cuatreros station. comprised 42% of the total amount of tintinnines at White station and almost 43% at Cuatreros during the spring peak (Table 3) and 48% at both stations during the summer peak (Table 3). Percentage abundance throughout the year of T. balechiis shown in Figure 4(a,b). Tintinnopsis brasiliensis. This species was present during almost the whole sampling period; it was absent from only some samples of August, November and December. Its annual mean abundance was 2821-1 at White station and 2991-1 at Cuatreros (Table 2). T. brasiliensis dominated during the fall peak, representing 49.5 and 59% of the total number of tintinnines at White and Cuatreros stations respectively (Table 3). M a x i m u m numbers attained were 2.5 x 1031-~ at White station and 3.5 x 1031-1 at Cuatreros. Tintinnopsis parva. Species of the genus Tintinnopsis are difficult to identify due to the great polymorphism of their loricae. In previous studies (Barria de Cao, 1981),' T. p a r v a ' a n d ' Tintinnopsis turbinata' were shown to exhibit gradual variation in lorica form from o n e ' species' to the other and they could not be clearly separated. Cultures and cytological studies are needed for a more precise taxonomy. I n this study, typical T. parva, intermediate forms and T. turbinata are all counted as ' T. parva '. This ' species ' was present throughout the year at both stations, with an annual mean abundance of 231 1-1 at White station and 271 1-1 at Cuatreros (Table 2). Highest numbers were recorded in summer

Abundance and species composition of Tintinnina

299

TABLE 2. Tintinnine species encountered in Bahia Blanca estuary and annual mean abundance (number of individuals I t) of dominant species

Tintinnidium balechi Tintinnidium sp. aft. semiciliatum Tintinnopsis brasiliensis Tintinnopsis gracilis Tintinnopsis glans Tintinnopsis parva Tintinnopsis baltica Tintinnopsis pusilla Tintinnopsis beroidea Tintinnopsis levigata Tintinnopsis compressa Tintinnopsis karajacensis Tintinnopsis parvula Tintinnopsis rotundata Tintinnopsis amphora Tintinnopsis buetschlii mortensenii Codonellopsis lusitanica Favella taraikaensis Metacylis sp. aft. mereschkowskyi

White station

Cuatreros station

488-9

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282 243 231.3 259.4

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Figure 3. Abundance of tintinnines during the 1986-87 period in Bahia Blanca estuary at White station (--) and Cuatreros station ( . . . . ). w i t h 1 x 1031- l in a s a m p l e o f D e c e m b e r at C u a t r e r o s . R e l a t i v e a b u n d a n c e d u r i n g t h e y e a r in t e r m s o f p e r c e n t a g e is s h o w n in F i g u r e 4(a,b). Tintinnopsis glans was p r e s e n t t h r o u g h o u t t h e year, w i t h an a n n u a l m e a n a b u n d a n c e o f 249 1- 1 at W h i t e a n d 259 1-1 at C u a t r e r o s ( T a b l e 2). T h i s species was also m o r e n u m e r o u s in s u m m e r ; it r e a c h e d a m a x i m u m o f a l m o s t 2 x 103 l - i in F e b r u a r y at W h i t e s t a t i o n a n d 0"9 x 1031- ~ in D e c e m b e r at C u a t r e r o s . R e l a t i v e a b u n d a n c e in t e r m s o f p e r c e n t a g e d u r i n g t h e s a m p l i n g p e r i o d is s h o w n in F i g u r e 4(a,b).

300

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TABLE 3. Species composition and percentage a b u n d a n c e d u r i n g peaks in a b u n d a n c e S u m m e r peak

Tintinnopsis baltica Tintinnopsis brasiliensis Tintinnopsis beroidea Tintinnopsis compressa Tintinnopsis glans Tintinnopsis gracilis Tintinnopsis parva Tintinnopsis paroula Tintinnopsis pusilla Tintinnopsis rotundata Tintinnoidium balechi Tintinnidium sp. aft. semiciliatum Codonellopsis lusitanica

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Cuatreros

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C ua t re ros

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42-8

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F i g u r e 4. Relative a b u n d a n c e of Tininnopsis parva ( ) Tintinnopsis glans ( - - . --) and Tintinnidium balechi (. . . . ) t h r o u g h o u t t he s a m p l i n g period, as percentages of t he total sample. (a) W h i t e station; (b) C ua t re ros station.

Abundance and speciescomposition of Tintinnina

301

Tintinnopsis gracilis is the species which exhibited a more clearly restricted seasonal distribution. It was present during spring, summer and fall and was absent during the winter. T. gracilis reached a maximum number of 1-1 x 1031-I at White station and 1.8 x 1031-i at Cuatreros during the summer peak in abundance, representing the second species in order of abundance after Tintinnidium balechi (Table 3). T. gracilis may be considered a summer/fall species with annual mean abundance 2431-1 at White and 2661- i at Cuatreros (Table 2). Tintinnopsis baltica was present during almost the whole sampling period. It was absent from only some samples of March, November and December, and was present throughout the winter period. T. baltica reached maximum abundance in spring with I x 1031-1 at White station and 1-1 x I031 -~ at Cuatreros and may be considered a winter/spring species. Annual mean abundance was 259 1-1 at White station and 265 1-1 at Cuatreros (Table 2). Tintinnopsis beroidea. This species mainly occurred during spring and summer, reaching maximum abundance of 0.6 x 1031-~ at White station in spring and 0.5 x 1031-1 at Cuatreros in summer. Its annual mean abundance was 101 1-i at White station and 701-1 at Cuatreros (Table 2). Tintinnopsis pusilla was frequent throughout the year but was not present in all samples and did not show a clear annual pattern. Maximum numbers were recorded in spring, namely 0.4x1031 -~ at White station and 0.6x1031 -t at Cuatreros. Annual mean abundance was 1321-~ at White station and 141 1-1 at Cuatreros (Table 2). Codonellopsis lusitanica. Like Tintinnopsis pusilla, C. lusitanica showed no obvious seasonal pattern; its maximum abundance in summer was 0-7 x 1031- ~ at White station and 0.8 x 1031-1 at Cuatreros. Annual mean abundance was 179 1-~ at White station and 185 1-1 at Cuatreros (Table 2). Other species of minor importance were Tintinnidium sp. aft. semiciliatum, Tintinnopsis levigata, Tintinnopsis compressa, Tintinnopsis rotundanta, Tintinnopsis parvula, Tintinnopsis karajacensis and Tintinnopsis amphora. T h e maximum abundance value for these species was 0.2 x 1031-1 reached by T. levigata which occurred mainly in the fall and spring. T. sp. aft. semiciliatum was recorded in all seasons, but never exceeded 0.1 x 1 0 3 l- 1 T. compressa was present in winter, spring and summer. T. parvula, T. karajacensis and T. rotundata were present in summer and fall. T. amphora was recorded from only a few samples in spring. A few other species, Favella taraikaensis, Tintinnopsis buetschlii mortensenii and Metacylis sp. aft. mereschkowskyi, which are typical species of the outer part of the estuary (Barria de Cao, 1986), were occasionally observed in the inner part. Of these, only F. taraikaensis was abundant on one occasion in winter when it reached a maximum abundance of 0"3 x 1031-1. F. taraikaensis was present in most samples in winter and in one sample in the fall. T. buetschlii mortensenii was recorded in two samples in the fall and in two samples in summer. Metacylis sp. aft. mereschkowskyi was found in only one sample in spring. Fragments of Tintinnopsis radix, another species typical of the outer part, were recorded from some samples in spring and fall. These loricae were not taken into account for abundance as only unbroken loricae were counted.

Discussion Both stations showed similar patterns in variation of temperature, salinity and abundance of tintinnines. Species composition was similar in each locality, with slightly higher annual mean abundances of the most dominant species at Cuatreros (Table 2).

302

M. S. Barria de Cao

T h e genus Tintinnopsis was the most numerous in terms of number of species, comprising 73.7% of total recorded species (Table 2). A similar species composition has been found by other authors in coastal environments (Konovalova & Rogachenko, 1974; Hedin, 1975; Hargraves, 1981; Paranjape, 1987; Sanders, 1987; Verity, 1987). Maximal numbers of 1041-1 are also common in estuarine and coastal waters (Vitiello, 1964; Konovalova & Rogachenko, 1974; Hargraves, 1981; Paranjape, 1987; Verity 1987). Therefore, with regard to species composition and abundance of tintinnines, the investigated area may be considered a typical estuarine environment. T h e presence of other species like F. taraikaensis which occur commonly in the outer part of the estuary, where there is more marine influence, indicates occasional intrusions of marine fauna. Changes in salinity from 25.9%0 to almost 41%o do not seem to influence the abundance or species composition of the tintinnine fauna. Tintinnine abundance was at a maximum in summer and early fall when temperatures were 23 and 16 °C respectively. Another peak in abundance was found in late winter early spring at a lower temperature, 12 °C, so there is no clear correlation of high numbers of tintinnines with temperature, except that abundance decreases with cold. Minimal abundances were registred at a minimum temperature of 8 °C. Broadly, however, it was found that at lower temperatures the n u m b e r of species decreased. A minimum of five species was found at 8.8 °C and a maximum of 13 species was found at 23 °C. Several studies report maximum abundance during spring, summer or fall (Konovalova & Rogachenko, 1974; Hedin, 1975; Kr~ini6, 1987b; Paranjape, 1987; Sanders, 1987; Verity, 1987). Vitiello (1964) found maximum abundance in the Bay of Algiers in winter, but the temperature during that period was relatively high (13-16 °C). According to Hargraves ( 1981 ), temperature is unlikely to directly cause changes in tintinnine abundance, but other factors such as specific thermal preferences, food supply and predators should be taken into account. Most of the studied species did not show a marked seasonal occurrence. Some species e.g.T, balechi, T. parva and T. glans were present throughout the year. Only three species, T. gracilis, T. baltica and T. beroidea exhibited marked seasonal changes in abundance. For a better understanding of abundance changes and seasonal distribution, further work is being carried out, particularly on the abundance of tintinnines correlated with nano-phytoplankton and net-phytoplankton chlorophyll a concentrations.

Acknowledgement We thank Miss Leticia Luro for drawing the figures.

References Balech, E. E. 1945Tintinnoinea de Quequ6n. Physis 20, 1-15. Balech, E. E. 1948 Tintinnoinea de Atl~ntida (R.O. del Uruguay). Communicaciones del Museo Argentino de Ciencias Naturales, Zoologia 7, 1-23. Balech, E. E. 1951 Nuevos datos sobre Tintinno!nea de Argentina y Uruguay. Physis 20, 291-302. Balech, E. E. 1964E1Plancton de Mar del Plata durante el periodo 1961-1962. Boletin del Instituto de Biologia Marina, Mar del Plata (Argentina) 4, 1-49. Barria de Cao, M. S. 1981 Contribuci6n al conocimientode los Tintinnoineos (Ciliata, Protozoa)de la zona de Bahia Blanca. Gontribuci6n Gientifica No. 61 del Instituto Argentino de Oceanografia ( I.A.D.O. ) , 1-70. Barria de Cao, M. S. 1986 Contribuci6n al conocimientode Tintinnina (Protozoa, Ciliophora) de la zona de Bahia Blanca(Argentina), II. Boletin del Instituto Espa~ol de Oceanografia 3, 143-150. Hargraves, P. E. 1981 Seasonal variations of tintinnids (Ciliophora: Oligotrichida) in Narragansett Bay, Rhode Island, U.S.A. Journal of Plankton Research 3, 81-91. Hedin, H. 1975On the ecologyoftintinnids on the Swedish west coast. Zonn 3, 125-140.

Abundance and species composition of Tintinnina

303

Konovalova, G. V. & Rogachenko, L. A. 1974 Species composition and population dynamics of planktonic infusorian (Tintinnina) in Amur Bay. Oceanology 14, 561-566. Kr~ini~, F. 1987a On the Ecology of Tintinnines in the Bay of Mali Ston (Eastern Adriatic). Estuarine, Coastal and Shelf Science 24, 401--408. Kr~inid, F. 1987b Tintinnines (Ciliophora, Oligotrichida, Tintinnina) in Eastern Adriatics Bays. Estuarine, Coastal and Shelf Science 24, 527-538. Paranjape, M. A. 1980 Occurrence and Significance of resting cysts in a Hyaline Tintinnid Helicostomella subulata (Ehre.) Jorgensen. Journal of Experimental Marine Biology and Ecology. Paranjape, M. A. 1987 The seasonal cycles and vertical distribution of tintirmines in Bedford Basin, Nova Scotia, Canada. Canadianffournal of Zoology 65, 41--48. Rassoulzadegan, F. 1979 Evolution armuelle des Cili~s p~lagiques en M6diterran6e nord-occidentale. II Cili~s Oligotrichs. Tintinnides (Tintinnina). Investigaci6n Pesquera 43, 417-448. Sanders, R. W. 1987 Tintinnids and other microzooplankton-seasonal distributions and relationships to resources and hydrography in a Maine estuary. Journal of Plankton Research 9, 65-77. Souto, S. 1970 Tintinidos de la costa atl/mtica entre los 31°y 35 ° de Latitud Sur (Uruguary y Sur de Brasil) (Protozoa, Ciliata). Physis 30, 187-208. Souto, S. 1973 Contribuci6n al conocimiento de los Tintinidos de agua dulce de la Rep. Argentina. I. Rio de la Plata y Delta del Paran/l. Physis, B 32, 249-254. Souto, S. 1974 Tintinidos del Rio de la Plata y su zona de influencia. Physis B 33, 201-205. Souto, S. 1974 Tintinidos subant~rticos del Mar Argentino (Protozoa, Ciliata). Physis 31,451-462. Verity, P. C. 1987 Abundance, Community Composition, Size distribution and Production Rates of Tintinnids in Narragansett Bay, Rhode Island. Estuarine, Coastal and Shelf Science 24, 671--690. Vitiello, P. 1964 Contribution a l'&ude des Tintirmides de la baie d'Alger. Pelagos2, 5--42.