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AQUATIC MICROBIAL ECOLOGY Published May 9 Aquat Microb Ecol l

Development and collapse of a Gymnodinium mikimotoi in the Seto Inland

Yasuo Nakamural,*,Shin-ya suzuki2, Juro ~iromi~

'National Institute for Environmental Studies, Tsukuba, Ibaraki 305, ZCollege of Agriculture and Veterinary Medicine. Nihon University. Fujisawa, Kanagawa 252. Japan

ABSTRACT. A red tide due to Gymnodinium mikimotoi () occurred at Harima-nada, the Seto (Japan), in summer 1995. Throughout the development and collapse of the red tide, abundance of G. mikimotoi and its potential predators (heterotrophic and ) was monitored daily together with environmental variables. While a nitrate and phosphate cline was pre- sent at around 15 m, G. mikimotoi concentrations increased rapidly for about a week In the subsurface layer (5 to 15 m) Then the population suddenly accumulated at the surface layer in the daytime and formed a red tide (ca 3 X 103 ml-'). Following the red tide formation, the abundance of naked het- erotrophic dinoflagellates (h-dlnos) started to Increase. Subsequently, the abundance of the tintlnnid c111ate Favella ehrenbergii increased (ca 10 ml-'1 and apparently consumed G. mikimotoj and h-dinos completely within a few days. On the basis of these results, the ecological differences between G. miki- motoi and Chattonella antiqua (Raphidophyceae; another representative red tide forming species in the Seto Inland Sea) are discussed, as well as the importance of microzooplankton grazing for the col- lapse of red tides.

KEYWORDS: Red tide Gymnodinium . Microzooplankton . Tintinnid . Heterotrophic dino- flagellate

INTRODUCTION dinium aureolum have been conducted (Honjo 1994 and references therein). However, to our knowledge, Gymnodinium mikinlotoi Miyake et Kominami ex no previous studies have dealt with the population Oda, conspecific with G. nagasakiense (Takayama & development and collapse of G. mikimotoi or G. aure- Matsuoka 1991), is a naked autotrophic olum on a daily basis together with the changes in and IS closely related to Gyroclinium aureolum (Hul- environmental variables and potential predators. We burt) (Partensky et al. 1988). While G. aureolum present here the wax and wane of a G. mikimotoi red blooms in the and in coastal waters around tide that occurred in the Seto Inland Sea in summer European countries, the United States and Argentina 1995, relative to the changes in environmental vari- (e.g. Pingree et al. 1975, Jones et al. 1982, Chang & ables (e.g. temperature, salinity, nutrients) and micro- Carpenter 1985, Jimenez et al. 1992, Negri et al. 1992), (heterotrophic dinoflagellate and ciliate) G. mikimotoi forms severe red tides in the coastal populations. The main aim of the present study was to waters around Japan and Korea during warm seasons explain the outbreak mechanisms of G. mikimotoi red (e.g. Iwasaki et al. 1990, Honjo 1994). Red tides by G. tide when the water was thermally stratified and to mikimotoi have killed farmed fish. For example, the assess the roles of microzooplankton populations in the damage reached 4.4 billion yen in a red tide which disappearance of the red tide. occurred in Kumano-nada, Japan, in 1984 (Honjo 1994). In the last 3 decades, many ecological and physio- METHODS logical studies on Gymnodinium mikimotoi and Gyro- In summer 1995 (15 July to 8 August), a field survey 'E-mail: [email protected] was conducted at Stn B (34" 35' N, 134"30' E, 21 m

O Inter-Research 1996 132 Aquat Microb Ec

depth; see Nakamura et al. 1993) around the Ie-shima fixed samples (2";))from 29 July (10 m) and 4 August Islands in the Seto Inland Sea. Water temperature, (0 m), respectively, using an inverted microscope salinity, and dissolved oxygen were monitored at 2.5 m (~2001. intervals using a Surveyor I1 (Hydrolab Co.). Water samples for chemical analysis [NO:;, NO2-, NH;, PO.,'., Si(OH),, chlorophyll a (chl a)]and Gymno- RESULTS dinium mikimotoi enunlerations were taken at depths of 0, 5, 10, 15 and 19 m using a 10 1 Van Dorn-type bot- Environmental conditions and development tle. Samples for microzooplankton enumeration were of the red tide taken at 0 and 10 m. Monitoring and sampling were conducted daily in the morning (06:20 to 07:OO h). Sam- The weather was sunny and calm throughout the ples for nutrients (100 ml) and chl a (500 ml) were fil- survey period except on 17 and 22 July, when some tered through GF/F filters immediately after sampling, precipitation was recorded. The water was thermally stored at -20°C, and analyzed after the completion of stratified (Flg. 1) and sa1ini.t~ranged between 30.3 and the field survey. Nutrients were analyzed with a Tech- 33.0 ppt. As the developmrmt of anoxic bottom water nicon Auto Analyzer I1 for PO," (Murphy & Riley has been suggested to play an important role in the 1962), NH4+(Sol6rzano 1969), NO2- (Bandschneider & development of Gymnodlnium mikimotoi red tides Robinson 1952), NOz- + No3- (Wood et al. 1967) and (Iizuka & lrie 1969, Iizuka 1972), it should be noted that Si(OH), (Strickland & Parsons 1968). Chl a was mea- dissolvcd oxygcn at 20 m depth (1 m above the bottom) sured fluorometrically (Yentsch & Menzel 1963). exceeded 4.0 ppm from 15 July to 5 August, with a Abundance of Gymnodinium mikimotoi was mea- minimum of 3.5 ppm on 8 August. sured by observing l m1 intact samples in a Sedge- The abundance of Gymnodinium mikimotoi aver- wick-Rafter chamber under a microscope within aged over the water column sta.rted to increase on 23 90 min after collection. Before enumeration, samples July, increased at a rate (0.63 d-l) close to 1 doubling were vigorously mixed to slow down the movement of d-', reached a maximum of 380 ml-' on 30 July, and G. mikimotoi cells. then sharply decreased (Fig. 2A). From 23 to 30 July Samples (80 ml) for microzooplankton enumeration when G. mikirnotoi concentrations increased, cells were fixed with glutaraldehyde (final conc.. l'!<,), were most abundant between depths of l0 and 15 m in

stored at 5OCfor 1 h and stained with DAPI (final conc.. the morning (Fig. 2B). A dense accumulation of cells in 1 pg ml-'; Porter & Feig 1980) Then subsamples of the surface layer (red tide) was not observed until the 20 m1 were concentrated onto 0.8 pm pore size black afternoon of 29 July. From 30 July to 3 August, G. miki- Nuclepore filters (25 mm 0) under low (

1000 Nutrients. Coupled with the thermal stratification A of the seawater, concentrations of nitrate and phos- phate were generally low at depths of 0 to 5 m. -F Clines for these nutrients were present in the 10 to VE 100 15 m layer when the Gymnodjnium mikimotoi popu- lation developed (Fig. 3A, B). The level of ammonium 0a, c was usually around 1 pM (Fig 3C), and a slight m increase was observed just after the collapse of the Uc l0 red tlde. Silicate was always higher than 13 PM a throughout the water column until 4 August, and mm. then decreased sharply to ca 3 PM at 0 to 10 m depth S July1So 14 19(\al 24 29 Aug. 3 m#• 8l (data not shown) in accordance with the development m@ of diatoms (see above).

Date

-- , July 15 20 25 30 Aug. 4 Date July 15 20 25 30 Aug. 4 Date

-v 8 July 15 20 25 30 Aug. 4 -" 1 July 15 20 25 30 Aug. 4 Date Date

Fig. 2. Red tide formed by Gymnodin~ummikimotoj. (A)Tem- poral changes in the abundance of G. mikimotoi (m]-') averaged over the water column; (B) vertical and temporal changes in the abundance of G. mikimotoi (ml-') and (C) chlorophyll a (pg 1-l). H: high; L: low

not shown). However, the phytoplankton was com- pletely dominated by Gymnodinium mikimotoi at depths of 10 to 15 m from 26 to 30 July, throughout the water column from 31 July to 1 August, and at 0 to 10 m 15 from 2 to 3 August. After the collapse of the G. miki- July 25 30 Aug. 4 motoi red tide, Chaetoceros spp. became dominant. Date Chl a was within the range 0.6 and 18.9 pg 1-' and the Fig. 3. Vertical and temporal changes in (A) nitrate (FM), (B) maximum was observed at 15 m on 30 July (Fig. 2C). phosphate (PM),and (C) ammonium (FM].H: high; L: low 134 Aquat Microh Ecol 10: 131- t37, 1996

Microzooplankton Ciliates. Oligotrichs were numerically abundant among naked ciliate populations. Cone-shaped mixo- Heterotrophic dinoflagellates. Throughout thesurvey trophic oligotrichs ca 40 pm and ca 90 pm in size tvere period, dominant species of naked h-dinos were Gyro- the dominant ciliates throughout the survey period and dinium domindns and G. spirale for the 20 to 40 and the smaller ciliates were more abundant. Although 2 >40 pm size classes, respectively, as confirmed by the peaks of naked ciliates were observed (20-24 July and observations of live samples. The abundance of naked 7-8 August), they did not respond to the outbreak of h-dinos was relatively constant during the period of red Gymnodinium mikimotoi red tide (Fig. 4C). Through- tide development, started to increase on 30 July (the out the red tide, naked ciliate cells with fluorescent red peak of Gymnodinium mikinlotoi abundance; cf. Fig. 2), food vacuoles (>l0 pm) were not observed. reached a peak on 2 August, and then decreased sharply In July, tintinnids were less abundant than naked cil- together with the collapse of the red tide (Fig. 4A, B). iate~,and cells with an oral lorica diameter of less than From 1 to 3 August, naked h-dinos that contained a large 30 pm were dominant. Favella ehrenbergii (ca 65 pm food vacuole (>l0 pm) with red autofluorescence were in oral lorica diameter; identified by Y. 0. Kim) was often observed (not precisely enumerated, but account- first observed on 31 July and accounted for >95'Y0 of ing for some 10 % of total naked h-dinos cells). tintinnid cilidte cells ml.' from 1 to 6 August. The The abundance of thecate h-dinos was much lower abundance of tintinnids started to increase sharply on than that of naked cells and no systematic trends were 31 July, reached a maximum on 3 August and then observed (data not shown). decreased (Fig. 49). F, ehrenbergji was abundant at

July14 19 24 29 Aug. 3 8 July 14 19 24 8 Date Date

July 14 19 24 29 Aug.3 8 July14 19 24 29 Aug. 3 8 Date Date

Fig. 4 Changes In the abundance (ml-') of (A) naked heterotrophic dinoflagellates with sizcs of 20 to 40 pm. (B)naked hetero- trophlc dinoflagellates with sizes of 40 to 200 pm. (C) naked ciliates with sizes of 20 to 200 pm, and (D) tlntinnids. (0)Values at 0 m;(0) values at 10 m; (-1 averaged values between 2 depths Nakalnura et al.. Development and collapse of a red tide

10 m in the morning but accumulated at the surface the nutrient cline) and takes up nutrients for growth. around noon (data not shown). From 31 July to 3 However, this scenario is applicable only when G. August most F. ehrenbergii cells were filled with food mikimotoi can take up nutrients at night. Nutrient vacuoles apparently originating from Gymnodiniurn uptake and growth kinetics of this species as a func- ~nikimotoi. tion of nutrient concentration and 1.ight conditions Ebria tripartid.The abundance of the heterotrophic deserve further study. silicoflagellate Ebria trjpartia (ca 35 pm) was high (2 to In the Seto Inland Sea, Chatlonella antiqua (Raphi- 4 ml-l) from 16 to 20 July when a diatom Skeletonema dophyceae) 1s another representative organism that costatun] was abundant, and decreased to

Collapse of the red tide bacteria increased from 3.0 X 10"nd 3.5 X 10ho 4.9 X lob and 5.9 X 105 ml-l, respectively, probably due to For the C;ymnndinium mikimotoi red tide of 1994, the decrease of grazing pressure by heterotrophic evidence was presented suggesting that h-dinos, espe- nanoflagellates. Thus, F. ehrenbergii seemed to affect cially Gyrodinium dominans and Gyrodinium spirale, the nano/pico-sized plankton community structure contributed significantly to its disappearance (Naka- directly or indirectly in our study area. mura et al. 1995b). In contrast, in the red tide of 1995. Our find~ngs stress the ecological importance of we conclude that the tintinnid ciliate Favella ehren- Favella ehrenbergii. However, questions still remain. bergii played a major role in the disappearance, based (1) Why did F. ehrenbergii not devlop during the red on the following considerations. First, the timing of the tide of 1994 (Nakamura et al. 1995b)? Was the initial collapse of the red tide and the rapid increase in F. abundance of F. ehrenbergii too low? (2) Although the ehrenbergii abundance overlapped. Furthermore, if red tide of 1995 disappeared by 7 August in the central we assume that the population of G. mikimotoi at the part of Harima-nada, why did it continue until mid peak [30 July; abundance = 380 ml-', equivalent spher- August in the coastal area of and ical diameter (ESD) = 19 pm1 was all converted to that without F. ehrenbergii (Nagai pers. comm.)? At present of F. ehrenbergii (ESD of the body = 49 pm) with a we do not have any clues that could allow us to answer gross growth efficiency of 0.4, the abundance of F. these questions. However, future studies on changes in ehrenbergii would attain 10 ml-', close to the observed the life cycle of F. ehrenbergii (e.g. timing of excyst- vaiue (Fig. 4D). Second, F. ehrenbergii cells were filled mcnt from the sediment) might help to explain these with large food vacuoles (>l0 pm) that fluoresced red issues. when G. mikimotoi was abundant, whereas after the disappearance of the red tide, no such vacuoles were Acknowledgements. We thank Drs Y 0. Kirn and R. Suzuki evident. Third, tintinnids can ingest particles up to for tintinnid species identification, and K. Suzuki and H. 45% of the oral lorica diameter (Spitter 1973, Hein- Kobayashi for support with the field sampling. This study was bokel 1978), and particles close to the maximum size supported by Grant-in-Aid No. 05640720 from the Scientific are usually ingested at higher rates than smaller parti- Research Fund of the Ministry of Education, Science and Cul- ture, Japan. cles (Rassoulzadegan 1978, Stoecker et al. 1995).Thus G. mikimotoi (28 X 27 X 9 pm; ESD = 19 pm) could be a suitable food item for F. ehrenbergii (oral diameter = ca 65 pm) Fourth, the body volume specific clearance LITERATURE CITED rate of tintinnids is ca 1 X 10' h-' (Neuer & Cowles Bandschneider K. Robinson RJ(1952) A new spectrophotomet- 1995), comparable to that of G. dominans (Nakamura ric determination of n~triteIn seawater. J marRes 11:87-96 et al. 1995a). Thus the clearance rate of F. ehrenbergii Bj~rnsenPK, Nielsen TG (1991) Decimeter scale heterogene- ity in the plankton during a pycnocline bloom of Gyro- (body volume = 6.2 X 104 pm3) is 6.2 p1 cell-' h-', suffi- dinium aureolum. Mar Ecol Prog Ser 73:263-267 cient to clear the G. mikimotoi population within a day Chang J, Carpenter EJ (1985) Blooms of the dinoflagellate if Favella abundance is 7 ml-' or above (Fig. 4D). Gyrodinium aureolum In a Long Island estuary: box model Although Hansen (1995) has pointed out that F. ehren- of bloom maintenance. marBiol 89:83-93 bergii cannot sustain its growth when fed Gyrodinium Dixon GK, Holligan PM (1989) Studies on the growth and aureolum (closely related to G. mikimotoi), we con- nitrogen assimilation of the bloom dinoflagellate Gyro- diniurn aureolum Hulburt. J Plankton Res 11:105-108 clude that F ehrenbergii ingested G. mikimotoi Hansen PJ (1995) Growth and grazing response of a ciliate actively, increased its abundance, and contributed to feeding on the red tide dinoflagellate Gyrodin~umaure- the disappearance of the red tide. 0th.er studies have olurn In monoculture and in mixture with a non-toxic alga. shown the importance of Favella sp. for controlling Mar Ecol Prog Ser 121:65-72 Heinbokel JF (1978) Stud~eson the functional role of tlntin- thecate dinoflagellates (Stoecker et al. 1984). nids in the Southern California Bight. I. Grazing and From 1 to 3 August, when Favella ehrenbergii con- growth rates in laboratory cultures. Mar Biol 47:177-189 centrations increased along with the decline in Honjo T (1994) The biology and prediction of representative Gymnodinjum mikimotoi (Fig. 4D), the plankton com- red t~desassociated with fish kills in Japan. Rev Fish Sci 2: munity structure also changed drastically. The abun- 225-253 Honjo T. Yamamoto S, Nakan~ura0, Yamaguchi M (1990) dance of h-dinos decreased rapidly (Fig. 4A, B) and Annual cycle of motile cells of Gymnodin~umnagasa- that of autotrophic and heterotrophic nanoflagellates kiense and ecological features during the period of red decreased from 2.0 X 103 and 2.2 X 10hl-' to 0.7 X 10" tide development. In Graneli E, Sundstrom B, Edler L, Anderson DM (eds)TOXIC manne phytoplankton. Elsevier, and 0.4 X 10hl-', respectively (S. Suzuki unpubl). New York, p 165-170 Although not conclusive, these changes seem to be lizuka S (1972) Gymnodinium type-'65 red tide occurring in due to ingestion by F, ehrenbergji. Furthermore, the anox~cenvironment of Omura Bay. Bull Plankton Soc abundance of heterotrophic bacteria and picocyano- Japan 19:22-33 Nakamura et al.: Development and collapse of a red tide 137

lizuka S, lrie H (1969) Anoxic status of bottom waters and lates Gyrodinium cf. aureolum and Gymnodinium nagasa- occurrences of Gymnodinium red water in Omura Bay. kiense. J Phycol 24:408-415 Bull Plankton Soc Japan 16:99-115 Pingree RD, Pugh PR, Holligan PM, Forster GR (1975) Sum- lizuka S, Mine K (1983) Maximum growth rate of Gymnodnium mer phytoplankton blooms and red tides along tidal fronts sp. (Type-'65), a red tide dinoflagellate, expected under in the approaches to the . Nature 258: culture conditions. Bull Plankton Soc Japan 30:139-146 672-677 Iwasaki H, I

Responsible Subject Editor: J. Dolan, Vdlefranche-sur-Mer, Manuscript first received: January 10, 1996 France Revised version accepted: March 13, 1996