Está en la página 1de 15

acta oecologica 32 (2007) 188202

available at

journal homepage:

Original article

Trends on the distribution of ciliates in the open Pacic Ocean

mez* Fernando Go
des Sciences et Technologies de LilledLille 1, FRE 2816 ELICO CNRS, Station Marine de Wimereux, Universite 28 avenue Foch, BP 80, F-62930 Wimereux, France

article info
Article history: Received 10 October 2006 Accepted 6 April 2007 Published online 11 June 2007 Keywords: Tintinnids Planktonic ciliates Oligotrichs Microzooplankton Microbial food web Grazing Pacic Ocean

The distribution of planktonic ciliates, aloricate (naked) and loricate (tintinnid) was investigated in the open waters of the Oyashio and Kuroshio Currents, Philippine, Sulu, Celebes and South China Seas, and the western and central equatorial Pacic. The abundance of nauplii and post-naupliar copepods as potential predators was estimated. In average, the tintinnids represented 1020% of the abundance of aloricate ciliates (50200 cells L1). One hundred and two species of 37 genera of tintinnids were recorded. As a general trend, the highest species richness was found in moderate oligotrophic waters. Photographic records of some taxa of interest and unidentied specimens were reported. In the subarctic waters of the Oyashio Current, a few tintinnid species showed high abundance uctuations that may be controlled by the copepods. During the summer the species of Parafavella with longer loricae predominated in parallel to the increase of the copepodite abundance. In warm open waters, the success of a ciliate species could depend on its anti-grazing strategy. Eutintinnus apertus attached to a spine-bearing diatom was the most ubiquitous species. Tintinnids may be subjected to lower predation pressure than aloricate ciliates. The increase of the lorica length or the association with diatoms may be an anti-grazing strategy, which determines the success of one tintinnid taxon versus other congeneric species. Although the aloricate ciliates would be less affected than tintinnids by the reduction of food availability under oligotrophic conditions, the ciliate populations as a general trend seem to be controlled by the predators (top-down) rather than by the availability of food resources (bottom-up). 2007 Elsevier Masson SAS. All rights reserved.



The microbial loop dominates in the stratied temperate and tropical open ocean. Pico- and nanoplankton are the dominant size fractions of phytoplankton in these oligotrophic systems and the microzooplankton plays a major role in the transfer of energy and material through the pelagic food web (Azam

et al., 1983). Ciliates and heterotrophic agellates are expected to be the main grazers since copepods are unable to crop these phytoplankton size classes efciently (Marshall, 1973). Planktonic ciliates are ubiquitous, and much attention has been given to their role as primary consumers of pico- and nanosized producers, as well as nutrient regenerators and important food sources of metazoan zooplankton and sh larvae

* Tel.: 33 3 21 9929 26; fax: 33 3 21 99 29 01. E-mail address: 1146-609X/$ see front matter 2007 Elsevier Masson SAS. All rights reserved. doi:10.1016/j.actao.2007.04.002

acta oecologica 32 (2007) 188202


(e.g. Pierce and Turner, 1992). Planktonic ciliates are a morphologically diverse group and are usually divided into loricate (tintinnid) and aloricate forms, often named as oligotrich or naked ciliates. The identication of aloricate ciliates requires slide mounting, cytological staining (i.e., protargol silver staining) and examination under high magnication (Montagnes and Lynn, 1987). The tintinnids can be identied based on lorica shape by examining specimens in plankton settling chambers. Most of the studies on planktonic ciliates, mainly tintinnids, have been performed in coastal waters. The composition of tintinnids has been investigated in the open eastern Pacic Ocean (Kofoid and Campbell, 1929, 1939; Balech, 1962) and the standing stocks of ciliates in the equatorial eastern Pacic (Beers and Stewart, 1971; Verity et al., 1996; Chavez et al., 1996), whereas the studies in the open western Pacic have been scarce (Hada, 1938; Taniguchi, 1977). Little is known about the spatial distribution and the factors that determine distribution. Beyond the scarce sample coverage in open waters, the comparison among the studies on planktonic ciliates is further complicated by the absence of standardization of the sampling methods and analytical protocols. Ciliates are delicate organisms and the results vary according to methodology such as sampling effort, sample collection, the concentrating method (bottles, horizontal or vertical net tows, direct or reverse net ltration of discrete samples and using nets of different mesh size, lters of different pore size, settling columns etc), xation method (Lugols or Bouins solutions, formalin), or microscope techniques applied (transmitted or epiuorescence, inverted or direct microscopy). For tintinnids, several genera are highly polymorphic and the criteria for the delimitation of the species may vary among the observers. The present study has been carried out by the same observer using the same methodology from a large set of

samples collected in several regions of the open western Pacic. Ciliates were enumerated in samples of settled whole waters, which yield signicantly higher ciliate cell counts than screened, sieved or net concentrated samples yield. This study is based on discrete depth samples rather than vertical hauls to give the vertical distribution. This allows the comparison of the composition and abundance of both aloricate and loricate, ciliates under different physical and trophic conditions. Simultaneously, the abundance of the early stages of copepods (all nauplii and post-naupliar forms) as main potential ciliate predators were estimated. Resource availability regulates the biomass on a trophic level from the bottom (bottom-up force) while the predation affects it from the top (top-down force). The trends have been examined with regard to the abundance of aloricate and loricate ciliates as potential competitors and the copepods as potential consumers of the planktonic ciliates. These relationships were examined in an attempt to determine factors directly related to the ciliate abundance and diversity in the open ocean.


Materials and methods

mez (2005) (Fig. 1). SamSample collection was described in Go ples of 400 ml were concentrated via sedimentation in glass cylinders. During a 6-day settling period, the top 350 ml of sample was slowly siphoned off with small-bore tubing. Fifty millilitres of concentrate representing 400 ml of whole water was settled in composite settling chambers. The entire chamber was scanned at 200 magnication with a Nikon inverted microscope equipped with a digital camera. The samples from the Oyashio Current were not pre-concentrated. The mechanical disturbance associated with sample collection and treatment very often provokes detachment of the soft cell body

Fig. 1 Map of the station locations marked by solid circles in the Pacic Ocean.


acta oecologica 32 (2007) 188202

from the loricae (Paranjape and Gold, 1982). Loricae with a cell body inside or intact loricae were enumerated. Broken loricae were not considered. During microscopical analysis, the undetermined species of tintinnids were photographed for further identication. Tintinnids were identied based on lorica characters by referring to Kofoid and Campbell (1929, 1939). It should be taken into account that Kofoid and Campbell rose to the rank of genus and species hundreds of tintinnids previously placed in lower categories. Ubiquitous genera such as Eutintinnus and Salpingella showed a pronounced polymorphism closely connected by intermediate forms, proving very difcult to draw any line of separation between the species of the genera. Here, a conservative approach was adopted, pooling apparent varieties. During this study, aloricate ciliates were enumerated, but not identied. Only the easily identiable species Myrionecta rubra (formerly Mesodinium rubrum) was enumerated separately. Copepod nauplii, all nauplii and post-naupliar stages pooled, were enumerated from the samples. Vertical hauls obviously provided a higher statistical precision in the estimation of the copepod abundance. However, the small fractions such as the naupliar stages may be inefciently retained and no information at discrete depths is provided. The present study provides an estimation of the abundance of nauplii and ciliates from the same samples. The data should be considered with caution due to the low sensitivity of this method. In some regions such as the Oyashio Current, data sets of zooplankton were summarized in the literature (e.g. Kobari et al., 2003).

were the most ubiquitous species, present in the 80% of stations. The aloricate ciliates were also abundant in the slope waters. In contrast to the tintinnids, the aloricate ciliates did not show a clear minimum in and under the Kuroshio Current. The aloricate ciliates were homogeneously distributed in the upper 100 m depth with values about 200 cells L1 (Fig. 2E). The nauplii and post-naupliar abundance showed a maximum in the slope waters. South of the Kuroshio Current, the naupliar stages were restricted to the uorescence maxima, as the vertical distribution was narrower than for the ciliates (Fig. 2F). More oligotrophic conditions prevailed in July (Fig. 2GI) and the abundance of aloricate ciliates decreased by about a factor of 2 from May to July (Fig. 2J). The vertical distribution of the ciliates was narrower than in May, mainly located between 50 and 100 m depth. (Fig. 2E, K). A total of 51 tintinnid species were recorded in the 144 samples analyzed. The most ubiquitous taxa were Salpingella spp., Protorhabdonella simplex, Parundela aculeata and Eutintinnus spp. (Table 1). In the north Philippine Sea, the abundance of nauplii was slightly higher in July than in May (Fig. 2L).


Celebes, Sulu and South China Seas



3.1. Kuroshio Current and north Philippine Sea (May and July)
Two cruises were carried out along the meridian 138 E in the south of Japan (Fig. 1). In May, a cyclonic gyre in slope waters made the Kuroshio Current narrower than in the July cruise (Fig. 2A) when the Kuroshio Current was wider and warmer (Fig. 2G). In May, the salinity of the Kuroshio Current (w34.7) did not differ from the surrounding offshore subtropical waters. In July, the Kuroshio Current was wider, warmer and the salinity was lower (<34.2) (Fig. 2B, H). In May, the uorescence was higher and shallower in the slope surface waters, while a deeper 7080 m depth maximum was present in the offshore subtropical waters. In July, the uorescence was lower in the slope waters than in May. Southward, in the Kuroshio Current, the uorescence values showed a deeper and thinner maxima at 90100 m depth (Fig. 2C, I). In May, the uorescence maximum in the slope waters was associated with the dominance of the tintinnid Epiplocyloides reticulata that reached an abundance of 1200 cells L1. The tintinnids were nearly absent in and under the Kuroshio Current. South of the Kuroshio Current, the tintinnid abundance was about 2030 cells L1 and homogeneously distributed in the upper 100 m depth (Fig. 2D). In total, 64 tintinnid species were identied from the 115 samples analyzed. Parundela aculeata, Epiplocyloides reticulata and Dadayiella ganymenes

Oligotrophic conditions prevailed in the open waters of the regional seas of the western Pacic Ocean. In the Celebes Sea, the surface water circulation through the Shibutu Strait that connects the Sulu and Celebes Seas induced wind-driven upwellings (see Takeda et al., 2007) (Fig. 3AC). The surface maxima of uorescence in the Celebes Sea were associated with an increase of the abundance of aloricate ciliates with a peak of 270 cells L1, whereas the abundance of tintinnids was low (Fig. 3D, E). In the south Sulu Sea, low salinity waters covered the surface layer (salinity <32.8) with surface temperature >28  C (Fig. 3A, B). The uorescence showed subsurface maxima about 50 m depth (Fig. 3C) that were associated with a slight increase of the tintinnid abundance (20 cells L1). A surface maximum of the tintinnid abundance was observed on the southern side of the Shibutu Strait (Fig. 3D). The abundance of aloricate ciliates showed homogenous values of about 20 50 cells L1 (Fig. 3E). The abundance of naupliar copepods showed a subsurface increase (Fig. 3F). The abundance of aloricate ciliates was low and inversely related to the abundance of nauplii. In the South China Sea, only one sampling station was visited. The abundance of tintinnids and ciliates was very low (<20 cells L1). A minimum in the abundance of ciliates was associated with a slight maximum of naupliar copepods (Fig. 3DF). During this study in the Celebes, Sulu and South China Seas, 42 tintinnid species were recorded from 81 samples. The most ubiquitous species were Eutintinnus apertus, Amphorides quadrilineata and Steenstrupiella steenstrupii.


Western and central equatorial Pacic Ocean

A longitudinal transect of 4400 km along the equator between 160 E and 160 W was investigated during El Nin o-Southern Oscillation conditions in January-February 2003. The Western Pacic Warm Pool, from 160 E to 170 W, was subdivided into two regions. From 160 E to 175 E, the uorescence showed

acta oecologica 32 (2007) 188202


Fig. 2 Section plots of (A and G) temperature ( C), (B and H) salinity, (C and I) uorescence (as relative units), (D and J) abundance of tintinnids (cells LL1), (E and K) abundance of aloricate ciliates (cells LL1), (F and L) abundance of nauplii (cells LL1). Left and right panels correspond to the distributions along the meridian 138 E in the south of Japan in May and July, respectively. a deep maximum (90120 m depth) (Fig. 3GI). The westernmost station (160 E) showed a slight maximum of the abundance of ciliates (100200 cells L1) and tintinnids (20 40 cells L1). The abundance of nauplii was very low (about 5 cells L1) (Fig. 3L). The abundance of ciliates decreased eastward. More oligotrophic conditions prevailed in the region between 175 E and in the frontal zone of the Equatorial Upwelling Region at 170 W in the eastern edge of the warm pool. The temperature was higher than 29.5  C and the salinity showed a minimum (<34.3) (Fig. 3H, I). The uorescence maxima were located at 100 m depth. The abundance of tintinnids was low with a slight deep maximum (20 cells L1). The abundance of aloricate ciliates was relatively homogeneous in the upper 100 m depth ranging from 50 to 100 cells L1. The abundance of nauplii was low and restricted to the deep uorescence maxima (Fig. 3L). The uorescence maxima were shallower in the Equatorial Upwelling Region (Fig. 3GI). The mesotrophic conditions of the eastern boundary of this region were not associated with a noticeable increase of the abundance of both aloricate ciliates and tintinnids, with the exception of a slight surface increase (150 cells L1 and 20 cells L1 for aloricate ciliates


acta oecologica 32 (2007) 188202

Table 1 List of tintinnid taxa recorded in the western Pacic Ocean. Location of the records: Kuro, Kuroshio Currentnorth Philippine Sea; Sulu, Sulu, Celebes and South China Seas; Equat, western and central equatorial Pacic; Oya, Oyashio Current off Hokkaido Taxon
Acanthostomella conicoides Kofoid et Campbell Acanthostomella minutissima Kofoid et Campbell Acanthostomella norvegica (Daday) Jrgensen (Fig. 6D) Albatrossiella ligera (Laackmann) Kofoid et Campbell Amphorellopsis quadrangula Kofoid et Campbell Amphorellopsis cf. tetragona (Jrgensen) Kofoid et Campbell Amphorellopsis sp. (Fig. 8D) ` de et Lachmann) Strand Amphorides amphora (Clapare ` de et Lachmann) Strand Amphorides quadrilineata (Clapare cf. Amplectella sp.-Cricundella (Fig. 8B) Ascampbelliella armilla (Kofoid et Campbell) Corliss Ascampbelliella protuberans Kofoid et Campbell (Fig. 8M) Ascampbelliella retusa (Hada) Corliss Ascampbelliella cf. urceolata (Ostenfeld) Kofoid et Campbell (Fig. 8C) Brandtiella palliata (Brandt) Kofoid et Campbell (Fig. 8F) Canthariella pyramidata (Jrgensen) Kofoid et Campbell Canthariella cf. septinaria Kofoid et Campbell Climacocylis cf. leospiralis Kofoid et Campbell (Fig. 8O) Climacocylis scalaria (Brandt) Jrgensen Climacocylis cf. scifo Kofoid et Campbell cf. Codonaria oceanica Brandt Codonella amphorella Biedermann Codonella cuspidata Kofoid et Campbell Codonella galea Haeckel Codonellopsis frigida Hada (Fig. 6C) Codonellopsis orthoceras (Haeckel) Jrgensen Codonellopsis pusilla (Cleve) Kofoid et Campbell Codonellopsis schabii (Brandt) Kofoid et Campbell Craterella aperta Marshall (Fig. 8N) Cyttarocylis eucecryphalus (Haeckel) Kofoid Dadayiella pachytoecus (Jrgensen) Kofoid et Campbell Dadayiella ganymenes (Entz) Kofoid et Campbell Dictyocysta elegans Ehrenberg Dictyocysta extensa Kofoid et Campbell Dictyocysta mitra Haeckel Epiplocylis deexa Kofoid et Campbell Epiplocylis undella (Ostenfeld et Schmidt) Jrgensen Epiplocyloides reticulata (Ostenfeld et Schmidt) Hada Eutintinnus apertus (Kofoid et Campbell) Kofoid et Campbell Eutintinnus elegans (Jrgensen) Kofoid et Campbell Eutintinnus fraknoii (Daday) Kofoid et Campbell Eutintinnus hasleaea Taniguchi et Hada (Fig. 8I-K) Eutintinnus lusus-undae (Entz) Kofoid et Campbell Eutintinnus pacicus (Kofoid et Campbell) Kofoid et Campbell Eutintinnus stramentus (Kofoid et Campbell) Kofoid et Campbell Eutintinnus tubulosus (Ostenfeld) Kofoid et Campbell Eutintinnus turgescens (Kofoid et Campbell) Kofoid et Campbell Ormosella trachelium (Jrgensen) Kofoid et Campbell Parafavella denticulata (Ehrenberg) Kofoid et Campbell (Fig. 6H) Parafavella joergensenii Hada (Fig. 6F, G) Parafavella ventricosa (Jrgensen) Kofoid et Campbell (Fig. 6I, J) Parundella aculeata Jrgensen Parundella longa Jrgensen Poroecus annulatus Kofoid et Campbell Poroecus apicatus Kofoid et Campbell Protorhabdonella curta (Cleve) Jrgensen Protorhabdonella mira Kofoid et Campbell Protorhabdonella simplex (Cleve) Jrgensen Protorhabdonella striatura Kofoid et Campbell Ptychocylis obtusa Brandt (Fig. 6E) Rhabdonella amor (Cleve) Brandt Rhabdonella cornucopia Kofoid et Campbell

Kuro May

Kuro July




acta oecologica 32 (2007) 188202


Table 1 (continued) Taxon

Rhabdonella elegans Jrgensen Rhabdonella spiralis (Fol) Brandt Rhabdonellopsis apophysata (Cleve) Brandt Rhabdonellopsis composita (Brandt) Kofoid et Campbell Rhabdonellopsis minima Kofoid et Campbell Salpingacantha perca Kofoid et Campbell Salpingacantha cf. unguiculata (Brandt) Kofoid et Campbell ` de et Lachmann) Jrgensen Salpingella acuminata (Clapare Salpingella attenuata Jrgensen Salpingella decurtata Jrgensen Salpingella faurei Kofoid et Campbell Salpingella cf. laminata Kofoid et Campbell Salpingella subconica Kofoid et Campbell Steenstrupiella gracilis (Jrgensen) Kofoid et Campbell Steenstrupiella intumescens (Jrgensen) Kofoid et Campbell ` de et Lachmann) Kofoid et Campbell Steenstrupiella steenstrupii (Clapare Stenosemella cf. nivalis (Meunier) Jrgensen Tintinnopsis beroidea Stein Tintinnopsis nucula (Fol) Brandt Tintinnopsis cf. campanula Daday Undella californiensis Kofoid et Campbell Undella claparedei (Entz) Daday Undella clevei Jrgensen Undella cf. hadai Balech Undella hyalina Daday cf. Undella sp. (Fig. 8E) Undella subcaudata Jrgensen Undellopsis-Amplectella unidentied (Fig. 8A) Unidentied truncate-cone tintinnid (Fig. 8L) cf. Xystonella acus (Brandt) Laackmann (Fig. 8G) Xystonella longicauda (Brandt) Brandt Xystonella trefortii (Daday) Laackmann Xystonellopsis brandtii (Lackmann) Jrgensen Xystonellopsis cymatica (Brandt) Jrgensen Xystonellopsis gaussii (Laackmann) Kofoid et Campbell Xystonellopsis paradoxa (Cleve) Jrgensen

Kuro May

Kuro July




a The spelling of the epithet of Eutintinnus haslae, derived from Dr. Grethe R. Hasle, has been corrected according to the article 31.1.2 of the ICZN.

and tintinnids, respectively). The abundance of naupliar copepods was higher in the Equatorial Upwelling Region (20 cells L1) (Fig. 3L). Forty-three species of tintinnids were identied from the 124 samples analyzed in the equatorial Pacic. The species Eutintinnus apertus, Rhabdonella amor and Steenstrupiella spp. (mainly S. gracilis) were encountered in the upper 80 m depth of all the stations. Rhabdonella elegans, Protorhadonella spp., Amphorides quadrilineata and Acanthostomella spp. were other common taxa. The species of the genera Undella and Parundella tended to be encountered in deeper waters. During the present study, Eutintinnus hasleae was exclusively recorded in the equatorial Pacic Ocean (Fig. 8HJ).


Oyashio Current

The Oyashio Current forms the western boundary of the subarctic circulation along the Kurile Islands. The region is characterized by high primary production and high zooplankton biomass (e.g. Shinada et al., 2001; Kobari et al., 2003). The

hydrographical conditions strongly differed from the previous regions investigated in the warm-open western Pacic. The surface temperature ranged from 1.5  C in April (station A7) to 15  C in August (station H) (Fig. 4). In the upper 200 m depth at station A7, the temperature showed the lowest values on April 14 (0.88  C at 90 m depth) and the highest temperature (6.61  C at 24 m depth) was recorded on May 10. On April 14, the assemblage of microphytoplankton was dominated by diatoms of the genus Chaetoceros with low values (400 cells L1). The microzooplankton was dominated by aloricate ciliates (770 cells L1), whereas the abundance of tintinnids was very low (<12 cells L1) with Ptychocylis obtusa (Fig. 6E), Codonellopsis frigida (Fig. 6C) and Parafavella sp. Large ciliates such as Laboea strobila, Myrionecta rubra (Fig. 6B) and other ciliates tentatively cf. Strombidium conicum or cf. Strombidium wulfi were abundant (Fig. 6A). The abundance of naupliar copepods was low. One week later, on April 22, the phytoplankton abundance increased the abundance to 50,000 cells L1 in an assemblage dominated of large diatoms (Thalassiosira spp. and Chaetoceros


acta oecologica 32 (2007) 188202

Fig. 3 Section plots of (A and G) temperature ( C), (B and H) salinity, (C and I) uorescence (as relative units), (D and J) abundance of tintinnids (cells LL1), (E and K) abundance of aloricate ciliates (cells LL1), (F and L) abundance of nauplii (cells LL1). Left panel: Celebes, Sulu and South China Seas; right panel: western and central equatorial Pacic. The interpolation of section plots in the SuluCelebesSouth China Seas should be considered cautiously because the numerous groups of islands make difcult to represent the results.

debilis). The abundance of aloricate ciliate showed a subsurface maximum (700 cells L1 at 25 m depth). Myrionecta rubra reached the highest values on April 22 with 380 cells L1 at 25 m depth. The tintinnid abundance increased to 125

cells L1, mainly due to P. obtusa followed by A. norvegica (Fig. 6D). On May 10, the physical conditions were slightly different, with saltier and warmer surface waters (Fig. 4). The

acta oecologica 32 (2007) 188202


Fig. 4 Upper panel: Vertical proles of temperature ( C) (thick solid line) and salinity (dotted). Lower panel: Vertical proles of the abundance of tintinnids expressed as cells LL1 (thin solid line with black circles) and aloricate ciliates (dotted line with solid squares) at station A7 and station H in the Oyashio Current off Hokkaido.

microphytoplankton was dominated by smaller species of Chaetoceros with an abundance of 60,000 cells L1. The tintinnids and aloricate ciliates showed similar values of abundance, with a higher abundance of aloricate ciliates near the surface (540 cells L1) (Fig. 4). One week later, on May 17, large diatoms such as Chaetoceros debilis and Thalassiosira nordenskioeldii were dominant and reached values of 180,000 cells L1. The abundance of aloricate ciliates was low and the tintinnids reached the highest abundance recorded in this study (2100 cells L1). The assemblage was dominated by P. obtusa (1250 cells L1), followed by A. norvegica and C. frigida (Fig. 5). The microscope observations revealed a high abundance of copepodite and adult copepod stages. In June and August the sampling was carried out at station H, located 30 km west of the station A7. The phytoplankton assemblage corresponded to post-bloom conditions of Chaetoceros debilis with low abundance (700 cells L1). The abundance of the tintinnids and aloricate ciliates showed a subsurface maximum with low values (100 cells L1 at 50 m depth). The species A. norvegica and C. frigida were nearly absent and P. joergensenii reached the highest abundance (Fig. 5). Another congeneric species such as P. denticulata (Fig. 6H), P. ventricosa (Fig. 6I, J) and Tintinnopsis spp. appeared. In late August, the microphytoplankton assemblage was composed of small species of Chaetoceros with a low abundance (500 cells L1). The vertical distribution of tintinnids and aloricate ciliates were nearly similar. Parafavella ventricosa was the dominant species.

The abundance of aloricate ciliates was slightly higher than the tintinnid, with values lower than 200 cells L1 (Fig. 5).


Trends on the abundance of ciliates

In the present study the percentage of tintinnids represented about 1020% of the abundance of aloricate ciliates. Taniguchi (1977) found average values of 1020 tintinnids L1 and 10 nauplii L1 along a latitudinal transect in the south Philippine Sea. The tintinnids showed a slight increase to 2040 cells L1 and the nauplii to 2060 cells L1 in the Celebes Sea. Taniguchi (1977) found abundances of 30, 121 and 50 cells L1 for aloricate, tintinnids and nauplii, respectively, in the south Philippine Sea and 50, 80 and 40 cells L1 for aloricate, tintinnids and nauplii, respectively, in the Celebes Sea. Taniguchi (1977) reported that the aloricate ciliate rarely exceeded the tintinnids, and both ciliates were comparable in number. In the eastern tropical Pacic Ocean, Beers and Stewart (1971) reported that the abundance of tintinnids was 26% of the abundance reported for aloricate ciliates. The relatively high proportion of tintinnids versus aloricate ciliates is higher than the values found in the present study (Fig. 2D, E, J, K and Fig. 3D, E, J, K). Beers and Stewart (1971) and Taniguchi (1977) were based on formalin-preserved samples. Karayanni et al. (2004) reported that in samples xed in Lugols solution


acta oecologica 32 (2007) 188202

Fig. 5 Histograms of the maximum abundance of some ciliate taxa in spring and summer at station A7 and H in the Oyashio Current off Hokkaido.

the abundance of aloricate ciliates was higher by a factor of 2 compared to formalin xation, whereas the tintinnids did not show any difference between the two treatments (Karayanni et al., 2004). Consequently the apparent lack of aloricate ciliates in the Celebes Sea or the higher proportion of tintinnids may depend on the methodology of these studies based on formalin samples that underrepresented the delicate aloricate ciliates. Ota and Taniguchi (2003) reported that the average abundance of total ciliates in the Okinawa Trough waters ranged from 40 to 250 cells L1. These values were similar to those recorded in other regions of the Pacic Ocean (Fig. 2E, K and Fig. 3E, K). In the East China Sea, Ota and Taniguchi (2003) reported that the tintinnid abundance compared to aloricate ciliates hardly exceed 10%. Vrs et al. (1995) based on epiuorescence microscopy reported an average abundance of 4000 cells L1 for ciliates or 40,000 cells L1 for heterotrophic dinoagellates at 110 W and 125 W meridians in the equatorial Pacic Ocean. From the same data set, Chavez et al. (1996) reported values of 3000 cells L1 for ciliates and >400,000 cells L1 for autotrophic dinoagellates with average values of chlorophyll a of 0.2 0.5 mg L1. These values are extremely high for open ocean waters. From the same surveys, Verity et al. (1996) reported average ciliate abundance of 39110 cells L1.


Trends on the tintinnid species richness

The estimation of species diversity based on different methodology and variable consideration of the lorica polymorphism or synonymy is necessarily accompanied by some degree of uncertainty in the comparison between different sets of data of tintinnid assemblages (Pierce and Turner, 1993). The species richness in different geographical areas should be compared based on the same methodology and sampling effort. In a 450 km latitudinal transect in the north Philippine Sea and Kuroshio Current, 64 and 51 species were encountered in May and July, respectively. The sampling effort, 5657 L, was similar in both cruises (Fig. 7). At rst sight, more eutrophic conditions in May versus July may favour the diversity and abundance of tintinnids. In the vicinity of the Kuroshio Current, several stations corresponded to slope waters. Consequently several neritic species, absent in other cruises in open waters, were here encountered. In the Celebes, Sulu and South China Seas, a total of 42 tintinnid species were

encountered. The sampling effort was only 22 L. In a longitudinal transect of 4400 km along the equatorial Pacic, 43 species were encountered from the 50 L examined (Fig. 7). Despite the lower sampling effort in the Celebes, Sulu and South China Seas, the relatively high tintinnid species richness may be explained by the higher diversity of hydrographical environments. The sampling in the equatorial Pacic was carried out during El Nin o conditions associated with homogenous and oligotrophic hydrographical conditions. At each station the number of species was high, with 2024 tintinnid species per station (Fig. 7). The hydrographical conditions were very similar among the stations in the Western Pacic Warm Pool and the same species tended to appear in stations separated more 550 km each one. One sampling station located in the north Philippine Sea (32 N, 138 E) with 26 species and other station in the equatorial Pacic (0 , 160 E) with 24 species showed the highest species richness. It is not assumed that temperature in warm waters was responsible for tintinnid diversity. The station in the Philippine Sea coincided with a surface peak of the nitrate and phosphate concentrations whereas the surrounding sta mez et al., 2005). This peak tions were nutrient-depleted (Go was associated with a slight increase of the uorescence, which suggested a recent nutrient enrichment event and an increase of the picoplankton and small nanoplankton abundance unnoticed by the present methodology. According to these results, a slight release of the oligotrophic conditions may favour an increase of the tintinnid species richness. The co-occurrence of ubiquitous tintinnid species, scarcely affected by environmental changes, together to other species favoured for the pulse of eutrophic conditions (available food), may be responsible of the increase of the species richness in these locations.


Trends on the composition of tintinnid species

Overall, 37 genera, comprising 102 species of tintinnids, were encountered (Table 1). Several undetermined taxa are shown in the Fig. 8. The most numerous genera were Eutintinnus (9 species), Undella (7) and Salpingella (6) (Table 1). The number of species within these genera depends on the criteria for the delimitation of the species and synonymy. For example, species of the genus Salpingella were encountered in nearly all the sampling stations, but in many cases the identication of species is further complicated by the existence of

acta oecologica 32 (2007) 188202


Fig. 6 Photomicrographs of ciliates from the vicinity of the Oyashio Current off Hokkaido, bright-eld optics. (A) Assemblage of aloriate ciliates in April. (B) Myrionecta rubra. (C) Codonellopsis frigida. (D) Acanthostomella norvegica. (E) Ptychocylis obtusa. (F, G) Parafavella joergensenii. (H) Parafavella denticulata. (I, J) Parafavella ventricosa. Scale bars [ 20 mm.


acta oecologica 32 (2007) 188202

Fig. 7 Distribution of the tintinnid species richness and sampling effort estimated as volume in litres of sample examined at each station along the meridian 138 E in the south of Japan in May (A) and July (B), Sulu-Celebes-South China Seas (C), and the western and central equatorial Pacic Ocean (D).

intermediate forms difcult to ascribe to one species or another. From the sampling of 40 stations in temperate and warm waters, the most ubiquitous species was Eutintinnus apertus, encountered in 30 stations. Amphorides quadrilineata was encountered in 24 stations, Ascampbelliella armilla, Dadayiella ganymenes and Protorhabdonella simplex in 22 stations and Parundella aculeata and Steenstrupiella steenstrupii in 19 stations. In open, warm waters numerous species were rare and it was difcult to establish endemism based on one or a few records. An exception was Eutintinnus hasleae, which was relatively common in deep waters (80200 m) from 160 E to 175 W along the equatorial Pacic. The rst record of this species, named as Eutintinnus sp., was in equatorial Pacic at 145 W (Hasle, 1960). Later Taniguchi and Hada (1981) described Eutintinnus hasleae from the marginal seas of the western tropical Pacic and Indian Oceans. Rhabdonella amor and Steenstrupiella gracilis were abundant in the equatorial Pacic and less common in other regions. The genus Dictyocysta was common in the vicinity of Kuroshio Current and marginal seas of the western Pacic, but in the present study this genus was not encountered in the equatorial Pacic. Stenosemella and

Tintinnopsis spp. were nearly absent in open waters. Stenosemella was only encountered in the slope waters of the south of Japan and Tintinnopsis in the Oyashio Current in summer. Several taxa showed a marked vertical distribution. Salpingella was encountered in surface waters, but they were common at subsurface depths. The species Protorhabdonella simplex and two species of Steenstrupiella (S. gracilis and S. steenstrupii) were distributed in the upper 80 m depth. Parundella aculeata tended to be found at subsurface depths (50150 m depth) in all temperate and tropical waters examined. Other species were rare and the records were restricted to deep waters, with examples such as Albatrossiella ligera, Brandtiella palliata, Ormosella trachelium, and in general the species of genera such as Amplectella and Undella (except the most common species, Undella clevei and U. claparedei, with a wider vertical distribution). The records of the genera Amplectellopsis and Cricundella were restricted to the original descriptions in the southeast Pacic Ocean (Pierce and Turner, 1993). If these genera are considered as valid and no aberrant forms of Amplectella or Undella, the Fig. 8B illustrates the rst record in the northern hemisphere.

Fig. 8 Photomicrographs of some rare or unidentied tintinnids from the open Pacic Ocean, bright-eld optics. (A) Undellopsis-Amplectella sp. (34 150 N, 138 E, 150 m). (B) Tentatively Cricundella or Amplectellopsis (33 N, 138 E, 90 m). (C) Unidentied tintinnid (33 N, 138 E, 80 m). (D) Amphorellopsis sp. (5 N, 121 E, 10 m). (E) cf. Undella sp. (7 N, 129 590 E, 50 m). (F) Brandtiella palliata (7 N, 129 590 E, 75 m). (G) Xystonella acus (41 300 N, 145 470 E, 10 m). (H) Unidentied tintinnid (33 N, 138 E, 30 m). (I) Eutintinnus hasleae (0 , 160 E, 100 m). (J) E. hasleae (0 , 175 W, 80 m). (K) E. hasleae (0 , 160 E, 200 m). (L) Unidentied tintinnid (33 N, 138 E, 5 m). (M) Ascampbelliella (Craterella) protuberans (33 N, 138 E, 70 m). (N) Craterella aperta (5 110 N, 124 050 E, 20 m). (O) Climacocylis cf. leiospiralis (7 250 N, 121 120 E, 20 m). Scale bars [ 20 mm.

acta oecologica 32 (2007) 188202



acta oecologica 32 (2007) 188202

Acanthostomella norgevica, Parafavella spp., Ptychocylis obtusa and Codonellopsis frigida were exclusively encountered the vicinity of the Oyashio Current (Fig. 6CJ). Acanthostomella norvegica and C. frigida appeared to be a better indicator of the cold waters of the Oyashio Current. Parafavella joergensenii appeared in spring, whereas the larger species of the genus were found in summer. According to Taniguchi (1983) P. joergensenii was not an appropriate indicator of the Oyashio Current. Boltovskoy et al. (1991) found in the Barents Sea only nine tintinnid species, where A. norvegica, P. obtusa and P. denticulata accounted nearly all the individuals. This assemblage, together with C. frigida was the same found in this study (Fig. 5CJ). Parafavella and Ptychocylis are exclusively arctoboreal genera, with the exception of the bipolar A. norvegica (Pierce and Turner, 1993).


Aloricate and tintinnid ciliates as competitors

Both aloricate ciliates and tintinnids are pico- or nanoplankton grazers and apparently compete for the same food resources. From several regions of the western Pacic Ocean, Suzuki et al. (1998) reported that the standing crop of ciliates was positively correlated to the biomass of nanoplankton. In the stratied open waters, larger nanoplankton and microplankton cells tend to be more abundant near the deep chlorophyll maxima. The present study revealed that during the summer in the north Philippine Sea the tintinnids were nearly restricted to the deep chlorophyll maximum, whereas the aloricate ciliates were more widely distributed in the upper 100 m depth (Fig. 2J, K). Investigations of feeding revealed that tintinnids ingest a large variety of picoand nano-sized prey, ranging in size from about 2 mm to particles about one half the lorica oral diameters (Spittler, 1973). Tintinnids have been shown to feed more efciently on nanoplankton (nanoagellates) than on picoplankton (Pitta et al., 2001). Aloricate ciliates such as Strombidium sulcatum preferentially grazed on picoplankton (Christaki et al., 1999). Pitta et al. (2001) reported that tintinnids ingested more prey than aloricate ciliates by a factor of 5. Taking into account that in the open warm waters the picoplankton is more ubiquitous that the nanoplankton, it can be expected that tintinnids may be more disfavoured than aloricate ciliates under oligotrophic conditions. In the present study the tintinnid abundance was low in very oligotrophic waters such as Kuroshio Current or Western Pacic Warm Pool, while the abundance of aloricate ciliates was less affected (Figs. 2 and 3). It can be expected that a tintinnid that needs to secrete and carry a lorica will require more preys than an aloricate ciliate of similar soft body biomass. Consequently, when the food availability is limited, a tintinnid would be more affected than an aloricate ciliate.


Predation on planktonic ciliates

Ciliates are important food sources for metazoan zooplankton and sh larvae (Pierce and Turner, 1992). Tintinnids are ciliates with a characteristic test (the lorica) secreted around the soft cell body. At rst sight, the extra cost of carrying a lorica, often with pointed extremes and sometimes spines, could provide an anti-grazing advantage. Eutintinnus or

Salpingella characterized by a transparent tubular lorica were the most widespread and species-rich genera. The main difference among the species was the size and shape of the loricae, often ared in the oral extreme and sometimes in the both extremes. Other common genera such as Xystonellopsis or Rhabdonella showed a more diversied lorica shape. Beyond the anti-grazing advantage, the lorica shape may increase the ow through the ciliary lter and consequent the clearance rate. The clearance rate of the tintinnids was 3 or 4 times higher than that of aloricate ciliates (Kivi and Seta la , 1995; Pitta et al., 2001). The most ubiquitous tintinnid in the western Pacic Ocean was Eutintinnus apertus. Its hyaline and non-ared lorica did not noticeably differ from other congeneric species. Eutintinnus apertus may benet by peculiar association with a short chain of Chaetoceros tetrastichon or Ch. dadayi, both diatoms mez, 2007). Consequently, with long spine-bearing setae (Go E. apertus could be less susceptible to predation than other Eutintinnus species. Assuming a nearly constant pico- and small nanoplankton abundance as food resources in the open ocean, tintinnid species less subjected to predation such as E. apertus will succeed versus other species. These features suggest that the ciliate populations in warm open ocean are controlled more by the differing susceptibility to predators than are controlled by the availability of resources. Although the aloricate ciliates would be less affected than tintinnids by the reduction of food availability under oligotrophic conditions, the ciliate populations as a general trend seem to be controlled by the different susceptibility to predators (topdown) than for the availability of resources (bottom-up). Beyond the warm-open ocean, the Oyashio Current with very high phytoplankton (resources) and copepods (predators) abundances constitutes a good laboratory to test the interactions of the predators and ciliate populations. In this study aloricate ciliates showed the higher abundance when copepods were absent (Fig. 5). A few species, Acanthostomella norgevica, Parafavella spp., Ptychocylis obtusa and Codonellopsis frigida were dominant in the entire subarctic waters (Boltovskoy et al., 1991). At rst sight, the temperature may be the main factor in selecting these few coldwater species. Acanthostomella norvegica and C. frigida showed a similar oral diameter (both about 25 mm) and length, 40 mm for A. norvegica and about 60 mm for C. frigida (Fig. 6). Both species, with similar distribution patterns, may apparently compete for the same food resources and are in the prey size spectra of the same predators. In the present study P. obtusa that appeared from April to August seemed to be adapted to different hydrographical conditions. The lorica oral diameter of P. obtusa was 6070 mm and the lorica length was about 100 mm, larger than the other two previous species. The species of the genus Parafavella appeared from April to August, with a higher abundance in summer. The smaller species of the genus such as P. joergensenii appeared in spring, whereas the larger species such as P. ventricosa with a lorica 300500 mm long were dominant in summer (Fig. 5). It may be interpreted that the succession of tintinnid species towards summer is associated with species of higher lorica length, whereas the oral diameter is nearly similar (4565 mm) (Fig. 6FJ). The dominant predators of ciliates in the Oyashio region are a few species of copepods of the genus Neocalanus. Gifford

acta oecologica 32 (2007) 188202


(1993) concluded that the species of Neocalanus were nonselective omnivores that consume microphytoplankton (>20 mm) and ciliate with equal efciency, obtaining 80% of its nutrition from protozoans. According to Kobari et al. (2003) Neocalanus accumulates a large amount of lipids in the surface layer, and then migrate down to the over-wintering depth to mature and reproduce without feeding. New generations produced at depth ascend to the surface layer where they utilize the seasonal peak of primary production. In the surface layer, a rapid increase in biomass occurred in early June when the young copepodite stage C5 was dominant. Kobari et al. (2003) reported that Eucalanus copepods in the Oyashio region fed non-selectively on nano- and micro-sized organisms, with diatoms the dominant food resource until May and ciliates after May. Based on this, a low grazing pressure can be expected in mid-April. According to this study, in mid-April the ciliate assemblage showed a high abundance of aloricate ciliates (Figs. 4 and 5). In May, the copepods reached the highest abundance and the aloricate ciliates were replaced by small tintinnids. At rst sight, it can be interpreted that tintinnids were more competitive than aloricate ciliates under a higher copepod grazing pressure. Through the summer, when the size and grazing of the copepods was higher (Kobari et al., 2003), these small tintinnid species were replaced by large species of Parafavella (Fig. 5). Ancient descriptions delimitated the Parafavella species by the number of oral denticles, being further considered a poor taxonomic criterion (Davis, 1978). In the subantarctic waters, Boltovskoy et al. (1990) investigated the intraspecic variability of Cymatocylis afnis/convallaria. Their results strongly suggest that both taxa, including the four formae into which C. afnis was originally divided, are members of a single species. Until further research is performed, the tentative morphotypes of Parafavella are considered separate species more than a single species that showed a seasonal elongation of lorica. Towards summer, the species of the genus Parafavella increase the length of the loricae and the pointed aboral process. The oral diameter of the Parafavella species, supposedly related to the prey size spectra, showed less difference (Fig. 6). It is uncertain whether the increase of the loricae length is a morphological adaptation of a single species in response to the predation by copepods or a selection of the larger species of the genus Parafavella.

food availability under oligotrophic conditions, the ciliate populations as a general trend seem to be controlled by the predators rather than by the availability of food resources.

This study was supported by a fellowship of the European Commission (ICB2-CT-200180002) held at the University of Tokyo with K. Furuya as host. I am grateful to the scientists and crew of R/V Soyo Maru (Nat. Res Inst. Fish. Sci.), R/V Hakuho Maru (ORI, Univ. Tokyo) and R/V Mirai (JAMSTEC), R/V Oshoro Maru (Hokkaido Univ.) and R/V Wakataka Maru (Tohoku Nat. Fish. Res. Inst.). Samples from stations H and A7 were provided by K. Kuma (Hokkaido Univ.), J Nishioka (CRIEPI) and S. Takeda (Univ. Tokyo). I thank M. Paine for assistance with English. This is a contribution to a Grant-in-aid for Creative Basic Research (12NP0201,DOBIS) from the MEXT, Japan and et Changement Global the French IFB Biodiversite programmes.




Predation, rather than competition for resources, has been hypothesized as a major factor for selecting plankton morphotypes (Verity and Smetacek, 1996) and such a hypothesis has been specically suggested also for the selection of tintinnid species (Capriulo et al., 1982). Based on the present study, the aloricate ciliates would be less affected than tintinnids by the reduction of food availability under oligotrophic conditions. Tintinnids may be subjected to lower predation pressure than aloricate ciliates. The increase of the lorica length or the association with diatoms may be an anti-grazing strategy, which determines the success of one tintinnid taxon versus other congeneric species. Although the aloricate ciliates would be less affected than tintinnids by the reduction of

Azam, F., Fenchel, T., Field, J., Meyer-Reil, R.A., Thingstad, F., 1983. The ecological role of water-column microbes in the sea. Mar. Ecol. Prog. Ser. 62, 4754. Balech, E., 1962. Tintinnoinea y dinoagellata del Pac co. Revista del Museo Argentino de Ciencias Naturales Bernardino gicas 8, 1249. Rivadavia. Ciencias Zoolo Beers, J.R., Stewart, G.L., 1971. Micro-zooplankters in the plankton communities of the upper waters of the eastern tropical Pacic. Deep-Sea Res. 18, 861883. Boltovskoy, D., Dinofrio, E.O., Alder, A.V., 1990. Intraspecic variability in Antarctic tintinnids the Cymatocylis afnis/ Cymatocylis convallaria species group. J. Plankton Res. 12, 403414. Boltovskoy, D., Vivequin, S.M., Swanberg, N.R., 1991. Vertical distribution of tintinnids and associated microplankton in the upper layer of the Barents Sea. Sarsia 76, 141151. Capriulo, G.M., Gold, K., Okubo, A., 1982. Evolution of the lorica in tintinnids: a possible selective advantage. Ann. Inst. anogr. Paris 58 (S), 319324. Oce Chavez, F.P., Buck, K.R., Service, S.K., Newton, J., Barber, R.T., 1996. Phytoplankton variability in the central and eastern tropical Pacic. Deep-Sea Res. II 43, 835870. Christaki, U., Jacquet, S., Dolan, J.R., Vaulot, D., Rassoulzadegan, F., 1999. Growth and grazing on Prochlorococcus and Synechococcus by two marine ciliates. Limnol. Oceanogr. 44, 5261. Davis, C.C., 1978. Variations of the lorica in the genus Parafavella (Protozoa: Tintinnida) in northern Norway waters. Can J Zool 56, 18221827. Gifford, D.J., 1993. Protozoa in the diets of Neocalanus spp. in the oceanic subarctic Pacic Ocean. Prog. Oceanogr. 32, 223237. mez, F., 2005. Histioneis (Dinophysiales, Dinophyceae) from the Go western Pacic Ocean. Bot. Mar. 48, 421425. mez, F., 2007. On the consortium of the tintinnid Go Eutintinnusand the diatom Chaetocerosin the Pacic Ocean. Mar. Biol. 151, 18991906. mez, F., Furuya, K., Takeda, S., 2005. Distribution of the Go cyanobacterium Richelia intracellularis as an epiphyte of the diatom Chaetoceros compressus in the western Pacic Ocean. J. Plankton Res. 27, 323330.


acta oecologica 32 (2007) 188202

Hada, Y., 1938. Studies on the Tintinnoinea from the western Tropical Pacic. J. Fac. Sci. Hokkaido Imp. Univ, ser. Zool. VI 2, 87190. Hasle, G.R., 1960. Phytoplankton and ciliate species from the tropical Pacic. Skrifter utgitt av Det Norske VidenskapsAkademi i Oslo. I. Matematisk-Naturvideskabelig klasse 2, 150. Karayanni, H., Christaki, U., Van Wambeke, F., Dalby, A.P., 2004. Evaluation of double formalin-Lugols xation in assessing number and biomass of ciliates: an example of estimations at mesoscale in NE Atlantic. J. Microbiol. Methods 56, 349358. Kivi, K., Seta la , O., 1995. Simultaneous measurement of food particle selection and clearance rates of planktonic aloricate ciliates (Ciliophora: Aloricateina). Mar. Ecol. Prog. Ser. 119, 125137. Kobari, T., Shinada, A., Tsuda, A., 2003. Functional roles of interzonal migrating mesozooplankton in the western subarctic. Pacic Prog. Oceanogr. 57, 279298. Kofoid, C.A., Campbell, A.S., 1929. A conspectus of the marine and fresh-water Ciliata belonging to the suborder Tintinnoinea, with descriptions of new species principally from the Agassiz Expedition to the Eastern Tropical Pacic 19041905. Univ. California Publ. Zool. 34, 1403. Kofoid, C.A., Campbell, A.S., 1939. The Ciliata: the Tintinnoinea. Bull. Mus. Comp. Zool. Harvard Coll. 84, 1473. Marshall, S.M., 1973. Respiration and feeding in copepods. Adv Mar. Biol. 11, 57120. Montagnes, D.W.S., Lynn, D.H., 1987. A quantitative protargol stain (QPS) for ciliates: a description of the method and tests of its quantitative nature. Mar. Microb. Food Webs 2, 8393. Ota, T., Taniguchi, A., 2003. Standing crop of planktonic ciliates in the East China Sea and their potential grazing impact and contribution to nutrient regeneration. Deep-Sea Res. II 50, 423442. Paranjape, M.A., Gold, K., 1982. Cultivation of marine pelagic anogr. Paris 58 (S), 143150. protozoa. Ann. Inst. Oce Pierce, R.W., Turner, J.T., 1992. Ecology of planktonic ciliates in marine food webs. Rev. Aquat. Sci. 6, 139181.

Pierce, R.W., Turner, J.T., 1993. Global biogeography of marine tintinnids. Mar. Ecol. Prog. Ser. 94, 1126. Pitta, P., Giannakourou, A., Christaki, U., 2001. Planktonic ciliates in the oligotrophic Mediterranean Sea: longitudinal trends of standing stocks, distributions and analysis of food vacuole contents. Aquat. Microb. Ecol. 24, 297311. Shinada, A., Ikeda, T., Ban, S., Tsuda, A., 2001. Seasonal dynamics of planktonic food chain in the Oyashio region, western subarctic Pacic. J. Plankton. Res. 23, 12371247. Spittler, P., 1973. Feeding experiments with tintinnids. Oikos 15, 128132. Suzuki, T., Yamada, N., Taniguchi, A., 1998. Standing crops of planktonic ciliates and nanoplankton in oceanic waters of the western Pacic. Aquat. Microb. Ecol. 14, 4958. Takeda, S., Ramaiah, N., Miki, M., Kondo, Y., Yamaguchi, Y., mez, F., Furuya, K., Takahashi, W., 2007. Biological Arii, Y., Go and chemical characteristics of high-chlorophyll, lowtemperature water observed near the Sulu Archipelago. DeepSea Res. II 54, 81102. Taniguchi, A., 1977. Distribution of microzooplankton in the Philippine Sea and the Celebes Sea in summer 1972. J. Oceanogr. Soc. Japan 33, 8289. Taniguchi, A., 1983. Microzooplankton distribution along a transverse section crossing a marked oceanic front. La Mer 21, 95101. Taniguchi, A., Hada, Y., 1981. Eutintinnus haslae n. sp., a new ciliated protozoa from the Tropical Pacic and Indian Oceans. La Mer 19, 1822. Verity, P.G., Smetacek, V., 1996. Organism life cycles, predation, and the structure of marine pelagic ecosystem. Mar. Ecol. Prog. Ser. 130, 277293. Verity, P.G., Stoecker, D.K., Sieracki, M.E., Nelson, J.R., 1996. Microzooplankton grazing of primary production at 140 W in the equatorial Pacic. Deep-Sea Res. II 43, 12271255. Vrs, N., Buck, K.R., Chavez, F.P., Eikrem, W., Hansen, L.E., stergaard, J.B., Thomsen, H.A., 1995. Nanoplankton of the equatorial Pacic with emphasis on the heterotrophic protists. Deep-Sea Res. II 42, 585595.