Chaetoceros Affinis Blooms in Palauan Meromictic Marine Lakes

Chaetoceros aﬀinis blooms in Palauan meromictic marine lake S. Konno, N. Inoue, D. U. Hernández-Becerril, R.W. Jordan

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S. Konno, N. Inoue, D. U. Hernández-Becerril, R.W. Jordan. Chaetoceros aﬀinis blooms in Palauan meromictic marine lake. Vie et Milieu / Life & Environment, Observatoire Océanologique - Laboratoire Arago, 2010, pp.257-264. hal-03262179

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Chaetoceros affinis blooms in palauan meromictic marine lakes

S. Konno 1, N. Inoue 2, D. U. Hernández-Becerril 3 , R. W. Jordan 4* 1 SCITA Center, Yamagata University, 1-4-12 Kojirakawa-machi, Yamagata 990 8560, Japan 2 Graduate School of Science & Engineering, Yamagata University, 1-4-12 Kojirakawa-machi, Yamagata 990-8560, Japan 3 Lab. Diversidad y Ecología del Fitoplancton Marino, Instituto de Ciencias del Mar y Limnología, Universidad Nacional Autónoma de México (UNAM), Apdo. postal 70-305, México, D.F. 04510, México 4 Department of Earth & Environmental Sciences, Faculty of Science, Yamagata University, 1-4-12 Kojirakawa-machi, Yamagata 990-8560, Japan * Corresponding author: [email protected]

CHAETOCEROS ABSTRACT. – Observations on net and water bottle samples obtained from marine lakes situated DIATOM BLOOM MARINE LAKE on Mecherchar Island in the Republic of Palau have revealed that Chaetoceros affinis commonly MEROMICTIC occurred in the meromictic lakes during 2001-2007, but was absent from the holomictic lakes and REPUBLIC OF PALAU lagoons. In Mecherchar Jellyfish Lake, C. affinis accounted for 42-93 % of the planktonic diatoms during most of the sampled years, representing up to 3.4 x 105 cells/liter. High relative abundances of C. affinis were also recorded from several other meromictic lakes during one of the sampled years, with an absolute abundance of 5.7 x 105 cells/liter (79 %) recorded in L-shaped Lake. These observations are the first record of planktonic diatom assemblages in Palauan meromictic marine lakes. The characteristics of these meromictic marine lakes and hypotheses for the recurrence of C. affinis blooms in Mecherchar Jellyfish Lake are discussed herein.

INTRODUCTION During the Pliocene and Pleistocene the uplift of Mio- cene carbonate platforms (coral reefs) resulted in a myriad The centric diatom genus Chaetoceros Ehrenberg con- of small ‘rock islands’ that now constitute the Palau archi- tains over 400 species (VanLandingham 1968, Kooistra pelago (Kelletat 1991). Subsequent erosion of the exposed et al. 2010), many of which live in coastal areas, produc- limestone, created a karst topography including a number ing high biomass blooms comprising long chains of cells of island basins. Today’s marine lakes were formed after and resting spores (Werner 1977). Although commonly the last glacial maximum (i.e. about 10,000 years ago), recorded from temperate and high latitude localities (e.g. when global sea level rose and the island basins became Rines & Hargraves 1987, Orlova & Selina 1993, Haecky filled with seawater, that had entered through cracks and et al. 1998, Sieracki et al. 1998, Booth et al. 2002, channels in the limestone. There are currently about 70 Shevchenko et al. 2006), high abundances have also been marine lakes in Palau, some of which are meromictic reported from subtropical and tropical regions, where (Hamner & Hauri 1981, Hamner & Hamner 1998). species such as C. amanita Cleve-Euler, C. ceratosporus Most of these Palauan lakes are surrounded by dense Ostenfeld, C. densus Cleve, C. elmorei Boyer, C. muel- forests of the red mangrove Rhizophora Linnaeus, but leri Lemmermann, C. salsugineus Takano, C. transisetus surprisingly few biological studies have been conduct- Johansen & Boyer and C. wighamii Brightwell may occur ed on the lake waters. In general, the meromictic lakes in estuarine waters or inland saline lakes (e.g. Brightwell have a three-layered water column; a productive epilim- 1856, Brunel 1962, Takano 1983, Rushforth & Johansen nion (mixolimnion) is separated from an unmixed anoxic 1986, Sanchez-Castillo et al. 1992, Johansen & Boyer hypolimnion (monimolimnion) by a thick layer of purple 1995, Trigueros et al. 2002, Oyama et al. 2005). photosynthetic sulphur bacteria (Chromatium Perty; There are thousands of saline lakes distributed around Venkateswaran et al. 1993) at the top of the chemocline the world (Mackenzie et al. 1995), many of which are (Fig. 1; see also the review by Lobban & Jordan 2010). non-marine. Most saline lakes are holomictic, monomic- The epilimnion is characterized by low diversity popula- tic or dimictic (well mixed or turning over once or twice tions of jellyfish (Hamner & Hauri 1981, Dawson 2005, a year, respectively), but true meromictic marine lakes Dawson & Hamner 2005), fish (Gotoh et al. 2009) and which incompletely or rarely turn over are relatively copepods (Saitoh et al. 2010), which differ from the scarce, possibly numbering less than 100 (Hamner & coastal and holomictic marine lake populations. Microal- Hamner 1998). At least 11 of these meromictic marine gal community studies in these lakes are almost non-exis- lakes are tropical, all of which are in the Republic of tent, with information solely from JFL, in which the phy- Palau, mostly located on Mecherchar Island – including toplankton was represented by chain-forming centric dia- the well known Mecherchar Jellyfish Lake (JFL). toms (e.g. Chaetoceros), large dinoflagellates (e.g. Cera- 258 S. KONNO, N. INOUE, D. U. HERNÁNDEZ-BECERRIL, R. W. JORDAN

Fig. 1. – Schematic representation of a Palauan meromictic marine lake, with mangroves around the lakeside, a mixolimnion characterized by jellyfish and planktonic diatoms, a thick bacterial layer of purple sulphur bacteria at the top of the chemocline, and an anoxic monimolimnion. Lake depth based on Mecherchar Jellyfish Lake. tium Schrank) and various microflagellates (Hamner et al. aluminium stub, coated with gold or platinum/palladium in an 1982). A more recent paper has recorded the presence of Eiko IB-3 ion sputter-coater and examined in a Hitachi S-2250N a new species of the diatom genus Paralia Heiberg in JFL scanning electron microscope. Photographs were taken with the (Konno & Jordan 2008). A few seaweed species inhabit camera attachment, using Fuji Neopan 120 SS black and white the shallower lakeside waters (Hara et al. 2002), while the film. In order to calculate absolute abundances, all of the dia- sediments from the shallower parts of JFL are known to tom frustules on the whole filter portion were counted. For those contain low diversity populations of benthic foraminifera filters with low abundances, counts of at least 300 diatom frus- (Lipps & Langer 1999, Kawagata et al. 2005a, b). tules were made on each water sample, however, the plankton In this study, we provide the first report on the plank- net samples were not quantified since the water volume passing tonic diatom communities of some of the meromictic through the net was unknown. All of the samples and negatives marine lakes of Mecherchar Island, and compare them used in this study are curated in the Department of Earth & Envi- with the communities in the island’s non-meromictic ronmental Sciences, Faculty of Science, Yamagata University. In general, the physico-chemical data were acquired using marine lakes and the surrounding lagoons. a multiple water-quality monitor (U-22, Horiba Co. Ltd.) at the same time as the water sample collection. However, on the three occasions when the monitor was broken, the water measurements MATERIALS AND METHODS were taken with a Hanna Instruments Piccolo Plus ATC Temp pH meter and a Shibuya Salinometer S-10 in July 2002, while con- Fieldwork in the Republic of Palau took place on eight occa- ductivity and salinity were measured with a Horiba Cond Meter sions between 2001-2007, with surface water samples taken ES-51, pH with a pH ep5 meter (Hanna Instruments), and tem- from a number of marine lakes on most trips, notably from perature and dissolved oxygen with a DO meter ID-100 (Iijima Mecherchar Island (see Fig. 2). Using a small boat, surface Electronics Corp.) in July 2005 and November 2006. No phys- water samples were also obtained from the lagoons surrounding ico-chemical data is available from 2004. The data for each of the larger islands, as well as from locations further offshore. In the lakes mentioned in this paper are documented in Hara et al. most cases the seawater was collected in plastic bottles (500 ml, (pers com). All the instruments were calibrated before the start of 1 l or 2 l), although during some of the earlier years the samples the fieldwork using commercially available standard solutions, were acquired with a Nytal-Swiss HD10 plankton net (mesh but due to logistical reasons (i.e. the difficulties associated with size 10 µm). Each water sample was filtered through a Milli- transporting equipment through the hot, dense jungle) they were pore® 47 mm, 0.45 µm porosity, HA-type polycarbonate filter not re-calibrated before taking measurements at each lake. using either a Nalgene® hand-operated vacuum pump or an Most of the informal names of Mecherchar Island lakes used A-3S Eyela Aspirator A-3S (Tokyo Rikakikai Co., Ltd.) filtra- in this paper are taken from Hamner & Hamner (1998), while tion apparatus. The filter was subsequently air dried and stored North Cassiopeia Lake and Cassiopeia Lake were named by in plastic petrislides for future SEM analysis. our research team due to the abundance in the lakes of ‘Upside At Yamagata University, a 3 x 3 mm (or 8 x 8 mm in earlier Down Jellyfish’ (belonging to the genus Cassiopeia Péron & years) portion of each filter was cut out and mounted onto an Lesueur).

Vie Milieu, 2010, 60 (3) CHAETOCEROS AFFINIS BLOOMS 259

in May and July 2002, 42.8 % in May 2003, and 92.9 % in October 2007 (see Table I). The only exception was in July 2005, when there was a low abundance of C. affinis (0.1 x 105 cells/liter; 6.7 % of the total diatom assemblage) and unusually high abundances of Hemiaulus hauckii Grunow and H. sinensis Greville (1.3 x 105 cells/liter and 0.5 x 105 cells/liter, or 67.4 % and 25.8 %, respectively). In the other meromictic lakes on Mecherchar Island, the planktonic diatom assemblages were sometimes dominated by C. affinis, for example in L-shaped Lake in October 2007, when C. affinis reached 5.7 x 105 cells/liter and represented 79.3 % of the total planktonic diatom assemblage. High relative abundances were also recorded in Clear Lake in May 2002 (84.3 %) and in Big Croco- dile Lake in May 2003 (45.3 %). However, Cyclotella spp. were more numerous in Big Crocodile Lake (79.9- 90.5 %) and Spooky Lake (91.8 %), particularly in Octo- ber 2007, and Actinocyclus spp. were common to dominant in Spooky Lake in May 2002 (94.7 %), May 2003 (94.4 %) and July 2005 (39.8 %), in Big Crocodile Lake in July 2002 (86.7 %), and to a lesser extent in L-shaped Lake in October 2007 (9.2 %). No other Chaetoceros species were found in the meromictic lakes, apart from in JFL in May 2003, when C. lorenzianus Grunow and an unidentified species occurred in low numbers. In the non-meromictic lakes that we were able to sample, the planktonic assemblages were quite different. For instance, Lake Ketau was dominated by Pseudosolenia calcar-avis (Schultze) Sundström in May 2002 (97.7 %) and by Bacteriastrum spp. in October 2007 (78.3 %), while North Cassiopeia Lake was dominated by Pseudo- solenia calcar-avis in October 2007 (61.5 %). Chaetoc- eros affinis was not recorded in any of these non-meromictic lakes. In the lagoons around Mecherchar Island Chaetoceros spp. only occurred in low abundances (< 104 cells/liter), with the highest abundances in the shallower areas outside the marine lakes. The commonest species were C. peruvi- anus Brightwell, C. convolutus Castracane, C. compres- sus Lauder, C. diversus Cleve and C. lorenzianus, while Fig. 2. – Maps of the (a) western North Pacific, (b) Republic of C. affinis was totally absent. Palau, and (c) Mecherchar Island (also arrowed in (b)). Num- bers in (c) refer to North Cassiopeia Lake (1), Cassiopeia Lake (2), Mecherchar Jellyfish Lake (3), L-shaped Lake (4), Big Description of C. affinis in the meromictic marine lakes Crocodile Lake (5), Crocodile Hole (6), Spooky Lake (7), Clear of Palau Lake (8), Little Crocodile Lake (9), Hot Water Lake (10), and Lake Ketau (11). Specimens of Chaetoceros affinis occur in long, straight chains (Figs 3-4), hundreds of microns long, and RESULTS over 10 µm wide. The setae of the terminal valves are either straight (Fig. 3) or strongly curved (Fig. 4), directed Planktonic diatom abundance in the Palauan marine at variable angles from the valve apices. Only the termi- lakes and lagoons nal valves possess a rimoportula. The terminal valve face margin is distinct and there is an indentation just above Chaetoceros affinis Lauder was the dominant plank- the thickened rim of the valve base (Figs 5, 8). The setae tonic diatom in JFL in most of the years we sampled (up of the terminal valve are significantly broader than those to 3.4 x 105 cells/liter), representing 42-93 % of the total of the intercalary valves (about 2 µm and < 1 µm, respec- diatom assemblage; 53.0 % in November 2001, 89.0 % tively), and although both bear spines, only those of the

Vie Milieu, 2010, 60 (3) 260 S. KONNO, N. INOUE, D. U. HERNÁNDEZ-BECERRIL, R. W. JORDAN

0.2 0.2 ‘07 Oct. 21.2 78.3

1 0.7 0.7 ‘02 Lake Ketau 97.7 May

1 L. 0.7 3.3 3.3 5.3 ‘02 84.3 May Clear

0.4 7.3 0.3 ‘07 Oct. 91.8

3.4 0.8 6.8 ‘05 July 23.7 25.4 39.8

1 3 Spooky L. 0.3 0.7 0.7 ‘03 94.4 May

0.3 0.7 1.3 2.7 ‘02 94.7 May

0.5 0.1 0.1 2.4 0.4 0.2 0.9 1.3 3.7 ‘07 Oct. 90.5

0.3 5.4 9.1 1.3 2.7 1.3 ‘05 July 79.9

5 0.3 0.3 0.7 ‘03 47.3 45.3 May

Big Crocodile L. 1 1 0.3 0.3 ‘02 July 10.7 86.7

L. 0.1 9.2 ‘07 11.4 79.3 October L-shaped

1 0.1 0.1 0.1 1.5 0.1 2.1 2.2 0.1 ‘07 Oct. 92.9

0.1 6.7 ‘05 July 67.4 25.8

3 4 12 0.7 8.7 2.3 4.3 7.7 0.3 2.3 ‘03 11.7 42.8 May

JFL 1 7 89 0.3 0.3 1.7 0.3 0.3 ‘02 July

1 1 1 89 7.3 0.7 ‘02 May

53 1.3 0.3 2.6 3.6 7.6 2.3 0.7 1.7 ‘01 10.3 16.6 ov. N ov.

L. 0.4 0.7 2.6 0.4 1.1 0.7 1.5 11.4 19.8 61.5 October ‘07 N . Cassiopeia

spp. spp. sp. spp. spp. spp. N itzschia spp. N avicula Psammodictyon spp. Araphids Cocconeis H emiaulus hauckii

Other raphids A mphora spp. Cyclotella H . sinensis Bacteriastrum spp. Paralia longispina Pseudosolenia calcar-avis C. lorenzianus Chaetoceros affinis Chaetoceros A ctinocyclus A ulacoseira T halassiosira spp. A chnanthes Chaetoceros spp. Chaetoceros Table I. – Relative abundances (%) of the main diatom taxa in the marine lakes of Mecherchar Island for the sampling period 2001-2007. period sampling the for Island Mecherchar of lakes marine the in taxa diatom main the of (%) abundances Relative – I. Table

Vie Milieu, 2010, 60 (3) CHAETOCEROS AFFINIS BLOOMS 261 intercalary setae appear to be spirally-arranged (Figs 6-7). incurved and stouter than the rest”. Since then, a num- The two types of setae also differ in morphology; the ber of subspecific taxa and similar-looking species have intercalary setae bear longitudinal rows of slit-like pores been described from around the World (e.g. Cleve 1873, (Fig. 6), whereas the terminal setae bear much fewer 1894, Schütt 1895, Gran 1897, Steeman-Nielsen 1931, pores, distributed somewhat randomly (Fig. 7). The inter- Thorrington-Smith 1970). However, Jensen & Moestrup calary setae of opposing valves often cross over close to (1998) showed that such diverse forms could be pro- the chain axis, before diverging (Figs 5, 9). Some of the duced from a single clone culture, suggesting that they intercalary cells had recently divided, with the aperture are not discrete taxa but environmental morphotypes of still covered by the mother cell wall (Fig. 8). the same taxon. Similarly, cultures of C. affinis isolated from Naples also exhibited high morphological variation (Hernández-Becerril 2004, unpub obs). Thus, we DISCUSSION have made no attempt to separate the forms of C. affinis in the Palauan meromictic lakes, since their basic valve Taxonomy and morphology of C. affinis morphology is identical, despite differences in the nature of the terminal valve, particularly the degree of curvature Lauder (1864) described Chaetoceros affine from of the setae and the angle at which the setae project from Hong Kong harbour as a new species with “terminal awns the valve apices – the main criteria often used to distin-

Figs 3-9. – Chaetoceros affinis. SEM micrographs. Fig. 3, chains of cells with straight terminal valve setae (L-shaped Lake, 2007). Fig. 4, chain of cells with curved terminal valve setae (JFL, 2007). Fig. 5, same specimen as in Fig. 4, showing close-up of terminal valve with its rimoportula. Note the difference in thickness between terminal and intercalary setae (JFL, 2007). Fig. 6, close-up of intercalary seta (JFL, July 2002). Fig. 7, same specimen as in Fig. 4, showing close-ups of the two types of setae (JFL, 2007). Fig. 8, recently divided cell with the mother cell wall still covering the aperture between the new valves (JFL, 2001). Fig. 9, chain of cells showing terminal valves, each bearing a rimoportula, in the middle of the chain (JFL, 2003).

Vie Milieu, 2010, 60 (3) 262 S. KONNO, N. INOUE, D. U. HERNÁNDEZ-BECERRIL, R. W. JORDAN guish C. affinis forms (e.g. Evensen & Hasle 1975, Rines Firstly, it is known from JFL sediment core analyses & Hargraves 1988, Hernández-Becerril 1996). that terrestrial plants, particularly mangroves, are the Some of the specimens from Palau have terminal major source of organic matter entering the lake (Orem et valves identical to those illustrated by Lauder (1864, pl. al. 1991, Lyons et al. 1996). Since it is known that phos- VIII, Fig. 5), i.e. with widely displaced setae that curve phates in aquatic systems originate from soils and decom- inwards in the distal portion (see our Fig. 4). Also, one posing leaf litter, and silicates are largely derived from of our specimens exhibits “intermediate awns” that “are weathered rocks, the nutrient supply in the lake is likely enlarged similar to the terminal ones” as noted by Lauder to be replenished by terrestrial run-off during periods of (1864). However, it is clear from our micrograph (Fig. 9) heavy rainfall (Wafar et al. 1997). that the ‘intermediate’ valves are actually terminal valves Secondly, significant amounts of nutrients are prob- prior to separation, as both valves possess a rimoportula ably being released into the mixolimnion by one or more (which is absent on intermediate valves). of the most abundant groups of organisms in the lake, i.e. the purple sulphur bacteria, the copepods and/or the Characteristics of a Palauan meromictic marine lake jellyfish. For instance, many species of purple sulphur bacteria are nitrogen-fixers. Furthermore, it has been sug- The tropical meromictic marine lakes of Palau appear gested that some pelagic copepods have such bacteria as to be unique, and therefore comparisons with other lakes part of their gut microbial flora (Proctor 1997). Thus the are difficult. The lakes have high water temperatures and co-existence of the bacteria and copepods in the Palauan salinities throughout the year (about 28-31°C and 26-29 meromictic lakes may be connected. Since Hamner et 5 2 PSU, respectively), and remain stratified due to the wind al. (1982) calculated as many as 3.2 x 10 copepods/m protection from the surrounding mangroves. They are in some of the lakes, such an association could be quite also effectively isolated from the surrounding ocean, as important. In addition, it is well known that marine cope- lagoonal waters entering the lake through the channels pods excrete copious amounts of ammonia when feeding on phytoplankton such as diatoms (Paffenhöfer & Gard- during high tide return to the lagoon after minimal mixing ner 1984), so the C. affinis blooms may be utilizing this as with the lake waters (Hamner et al. 1982). These limno- one of their main sources of nitrogen. On the other hand, logical conditions, together with the presence of the man- although nitrogen excreted by jellyfish can be readily used groves, bacterial layers, copepods and jellyfish, appear to by phytoplankton, it has been shown that jellyfish host- be beneficial to the growth of C. affinis. However, at pres- ing zooxanthellae release much smaller amounts of nitro- ent we have been unable to determine why this diatom is gen than those without zooxanthellae (Pitt et al. 2005). successful at growing in the meromictic lakes, but does Thus, it is likely that the Mastigias jellyfish in JFL, that not grow so well or is totally absent in the lagoons or non- host dinoflagellates as endosymbionts, are not the major meromictic lakes. Clearly, all the biological components source of the nitrogen used by the C. affinis blooms. in this unique lake ecosystem, as depicted in Fig. 1, are in Thirdly, it was recently suggested that the induced need of further study. drift of swimming jellyfish in a Palauan marine lake is a major contributor to water mixing, comparable to physi- Why do C. affinis blooms recur in Mecherchar Jellyfish cal processes such as winds and tides (Katija & Dabiri Lake? 2009). Given that i) these marine lakes are largely shel- tered from the wind due to the surrounding jungle, ii) Chaetoceros blooms occurring in temperate and sub- tidal influence is limited as evidenced by the persistent polar regions in spring are usually associated with high lake stratification, and iii) the jellyfish are nearly always nutrient concentrations, and increasing surface water present in large numbers, induced drift may be one of the temperature and light intensity, while post-bloom resting main mechanisms responsible for the biomixing of nutri- spore formation may be triggered by unfavorable condi- ents. This may be particularly true for Mecherchar Jel- tions such as nutrient depletion and decreases in surface lyfish Lake, where the numbers of resident jellyfish are water temperature and light intensity (Smetacek 1985, usually very high (up to 1.5 million individuals according Odate & Maita 1990). However, strong seasonal differ- to Dawson et al. 2001), apart from in La Niña years when ences are unlikely to occur in tropical localities such as their numbers may be drastically reduced due to stronger Palau. In fact, the Palauan meromictic marine lakes are water stratification associated with increased water tem- quite productive and constant all year-round, although peratures and higher rainfall (Martin et al. 2006). Thus it nutrient levels are relatively low (Hamner et al. 1982, would be interesting to see whether the C. affinis abun- Landing et al. 1991), presumably due to phytoplankton dance is equally affected by such an event. In July 2005 uptake. we did note a drastic reduction in C. affinis abundance, So where do the nutrients come from to support such prior to a period of extreme rainfall in November that was recurrent diatom blooms? Three hypotheses are suggested associated with a weak La Niña event (Wang & Watkins below. 2006), but there was no drop in the jellyfish numbers at

Vie Milieu, 2010, 60 (3) CHAETOCEROS AFFINIS BLOOMS 263 that time. Thus it is important that future monitoring of Cleve PT 1894. Redogörelse för de svenska hydrografiska these marine lakes encompasses as many plankton groups undersökningarne åren 1893-1894. II. Planktonundersök- ningar, Cilioflagellater och Diatomacéer. Bih Kongl Svenska as possible, to determine whether there are any clear links Vet-Akad Handl 20(III, 2): 1-16. to ENSO-related climate change. Dawson MN 2005. Five new subspecies of Mastigias (Scypho- Lastly, it is possible that species-specific grazing by zoa: Rhizostomeae: Mastigiidae) from marine lakes, Palau, copepods and other microzooplankton herbivores could Micronesia. J Mar Biol Ass UK 85: 679-694. lead to preferential increases of species that are not ingest- Dawson MN, Hamner WM 2005. Rapid evolutionary radiation ed. However, numerous studies have shown that Chaeto- of marine zooplankton in peripheral environments. P Natl ceros cells are not immune from copepod grazing and in Acad Sci USA 102: 9087-9430. fact they are sometimes the preferred choice of food when Dawson MN, Martin LE, Penland LK 2001. Jellyfish swarms, tourists, and the Christ-child. Hydrobiologia 451: 131-144. mixed populations are present (e.g. Schnack 1979). It has also been suggested that nutrients regenerated by grazers Evensen DL, Hasle GR 1975. The morphology of some Chaeto- ceros (Bacillariophyceae) species as seen in the electron may lead to blooms of lake phytoplankton (Porter 1976). microscopes. Nova Hedwigia Beih 53: 153-184. In summary, we have hypothesized that the recurrent Gotoh RO, Sekimoto H, Chiba SN, Hanzawa N 2009. Peripatric Chaetoceros affinis blooms in Mecherchar Jellyfish Lake differentiation among adjacent marine lake and lagoon popu- may be supported by the run-off of nutrients from the lations of a coastal fish, Sphaeramia orbicularis (Apogoni- lakeside soils and mangroves, the additional contribution dae, Perciformes, Teleostei). Genes Genet Syst 84: 287-295. of nitrogen compounds from the in situ purple sulphur Gran HH 1897. Protophyta: Diatomaceae, Silicoflagellata og Den Norske Nordhavs Exped 1876-1878, Bot bacteria and/or copepods, and the stirring of the nutri- Cilioflagellata. Protophyta 24: 1-36, pls 1-4. ents by the swimming motion of the resident jellyfish. It Haecky P, Jonsson S, Andersson A 1998. Influence of sea ice on is hoped that further studies will provide us with a more the composition of the spring phytoplankton bloom in the detailed picture of the diatom ecology and nutrient condi- northern Baltic Sea. Polar Biol 20: 1-8. tions of these Palauan meromictic marine lakes. Hamner WM, Gilmer RW, Hamner PP 1982. The physical, chemical, and biological characteristics of a stratified, saline, Acknowledgements . - The authors would like to sulfide lake in Palau. Limnol Oceanogr 27: 896-909. thank R Genka, K Ishii, S Ishizaka, Y Katsurada, Hamner WM, Hamner PP 1998. Stratified marine lakes of Palau C Komuro and K Oguchi (Yamagata University) for their (Western Caroline Islands). Phys Geogr 19(3): 175-220. help in the collection of the water samples, T Miya and Hamner WM, Hauri IR 1981. Long-distance horizontal migra- H Chiba (Yamagata University) for taking the water mea- tions of zooplankton (Scyphomedusae: Mastigias). Limnol surements in November 2001 and May 2002 respectively, Oceanogr 26: 414-423. and Marino and Ului (Carp Corporation, Koror, Palau) for Hara Y, Horiguchi T, Hanzawa N, Ishida K, Yokoyama A, their guidance and cooperation during the expeditions to Hoshina R, Kudoh H, Ochi A, Konno M 2002. The phyloge- Palau. This research was partially funded by two Grant- ny of marine microalgae from Palau’s marine lakes. Kaiyo in-Aids from the Ministry of Education, Science and Cul- Monthly 29: 19-26 [in Japanese]. ture of Japan, awarded to Professor Y Hara (13304065) Hernández-Becerril DU 1996. A morphological study of and Professor H Tamate (18405015) of the Department of Chaetoceros species (Bacillariophyta) from the plankton of Biology (Yamagata University), of which RWJ was a co- the Pacific Ocean of Mexico. Bull Nat Hist Mus London Bot recipient. The authors would also like to thank Professor 26: 1-73. N Hanzawa (Department of Biology, Yamagata Universi- Jensen KG, Moestrup Ø 1998. The genus Chaetoceros (Bacil- ty) for allowing SK to participate in the 2004 and 2005 lariophyceae) in inner Danish coastal waters. Opera Bot 133: expeditions. The revised manuscript benefited signifi- 1-68. cantly from the comments and suggestions of two anony- Johansen JR, Boyer JS Jr 1995. A morphometric analysis of six mous reviewers. Chaetoceros strains from inland saline lakes, with a description of Chaetoceros transisetus sp. nov. In Kociolek JP, Sul- livan MJ eds, A century of diatom research in North America: a tribute to the distinguished careers of Charles W. Reimer REFERENCES and Ruth Patrick. Koeltz Scientific Books, USA: 87-101. Katija K, Dabiri JO 2009. A viscosity-enhanced mechanism for Booth BC, Larouche P, Bélanger S, Klein B, Amiel D, Mei Z-P biogenic ocean mixing. Nature 460: 624-626. 2002. Dynamics of Chaetoceros socialis blooms in the North Kawagata S, Yamasaki M, Genka R, Jordan RW 2005a. Shal- Water. Deep-Sea Res Part II 49: 5003-5025. low-water benthic foraminifers from Mecherchar Jellyfish Brightwell T 1856. On the filamentous, long-horned Diatomace- Lake (Ongerul Tketau Uet), Palau. Micronesica 37: 215-233. ae, with a description of two new species. Q J Microsc Sci 4: Kawagata S, Yamasaki M, Jordan RW 2005b. Acarotrochus lob- 105-109. ulatus, a new genus and species of shallow-water foraminifer Brunel J 1962. Le phytoplancton de la Baie des Chaleurs. 2nd from Mecherchar Jellyfish Lake, Palau, NW Equatorial édit. Les Presses de l’Université de Montréal. Pacific Ocean. J Foramin Res 35: 44-49. Cleve PT 1873. Examination of diatoms found on the surface of Kelletat D 1991. Main trends of Palau Islands’ coastal evolu- the Sea of Java. Bih Kongl Svenska Vet-Akad Handl 1(11): tion, identified by air and ground truthing. GeoJournal 24: 1-13. 77-85.

Vie Milieu, 2010, 60 (3) 264 S. KONNO, N. INOUE, D. U. HERNÁNDEZ-BECERRIL, R. W. JORDAN

Konno S, Jordan, RW 2008. Paralia longispina sp. nov., an Rines JEB, Hargraves PE 1987. The seasonal distribution of the extant species from Palau and Haha-jima, western North marine diatom genus Chaetoceros Ehr. in Narragansett Bay, Pacific. In Likhoshway Y ed, Proceedings of the Nineteenth Rhode Island (1981-1982). J Plankton Res 9: 917-933. International Diatom Symposium. Biopress Ltd: 55-69. Rines JEB, Hargraves PE 1988. The Chaetoceros Ehrenberg Kooistra WHCF, Sarno D, Hernández-Becerril DU, Assmy P, Di (Bacillariophyceae) flora of Narragansett Bay, Rhode Island, Prisco C, Montresor M 2010. Comparative molecular and USA. Bibl Phycol 79: 1-196. morphological phylogenetic analyses of taxa in the Chaetoc- Rushforth SR, Johansen JR 1986. The inland Chaetoceros erotaceae (Bacillariophyta). Phycologia 49: 471-500. (Bacillariophyceae) species of North America. J Phycol 22: Landing WM, Burnett WC, Lyons WB, Orem WH 1991. Nutri- 441-448. ent cycling and the biogeochemistry of manganese, iron, and Saitoh S, Suzuki H, Hanzawa N, Tamate HB, in press. Species zinc in Jellyfish Lake, Palau. Limnol Oceanogr 36: 515-525. diversity and community structure of pelagic copepods in the Lauder HS 1864. Remarks on the marine Diatomaceae found at marine lakes of Palau. Hydrobiologia doi: 10.1007/s10750- Hong Kong, with descriptions of new species. Trans Microsc 010-0095-0. Soc Lond new ser 12: 75-79. Sánchez Castillo PM, Ubierna León MA, Round FE 1992. Estu- Lipps JH, Langer MR 1999. Benthic foraminifera from the mer- dio de Chaetoceros wighamii Brightwell: un taxon mal inter- omictic Mecherchar Jellyfish Lake, Palau (western Pacific). pretado. Diat Res 7: 127-136. Micropaleontology 45: 278-284. Schnack SB 1979. Feeding of Calanus helgolandicus on phyto- Lobban CS, Jordan RW 2010. Diatoms on coral reefs and in plankton mixtures. Mar Ecol Prog Ser 1: 41-47. tropical marine lakes. In Smol JP, Stoermer EF eds, The dia- Schütt F 1895. Arten von Chaetoceros und Peragallia. Ein Bei- toms: applications for the environmental and Earth sciences, trag zur Hochseeflora. Ber Deut Bot Ges 13: 35-48. 2nd edit. Cambridge University Press, Cambridge, UK: 346- 356. Shevchenko OG, Orlova TY, Hernández-Becerril DU 2006. The genus Chaetoceros (Bacillariophyta) from Peter the Great Lyons WB, Lent RM, Burnett WC, Chin P, Landing WM, Orem Bay, Sea of Japan. Bot Mar 49: 236-258. WH, McArthur JM 1996. Jellyfish Lake, Palau: Regenera- tion of C, N, Si, and P in anoxic marine lake sediments. Lim- Sieracki ME, Gifford DJ, Gallager SM, Davis CS 1998. Ecology nol Oceanogr 41: 1394-1403. of a Chaetoceros socialis Lauder patch on Georges Bank: distribution, microbial associations, and grazing losses. Mackenzie FT, Vink S, Wollast R, Chou L 1995. Comparative Oceanography 11: 30-35. geochemistry of marine saline lakes. In Lerman A, Imboden D & Gat J eds, Physics and chemistry of lakes. Springer-Ver- Smetacek VS 1985. Role of sinking in diatom life-history lag, New York: 265-278. cycles: ecological, evolutionary and geological significance. Mar Biol 84: 239-251. Martin LE, Dawson MN, Bell LJ, Colin PL 2005. Marine lake ecosystem dynamics illustrate ENSO variation in the tropical Steemann-Nielsen E 1931. Einige Planktonalgen aus den war- western Pacific. Biol Lett 2: 144-147. men Meeren 1. Dansk Bot Ark 6: 1-13. Odate T, Maita Y 1990. Seasonal distribution and vertical flux Takano H 1983. New and rare diatoms from Japanese waters. X. of resting spores of Chaetoceros (Bacillariophyceae) species A new Chaetoceros common in estuaries. Bull Tokai Reg in the neritic water of Funka Bay, Japan. Bull Fac Fish Hok- Fish Res Lab 110:1-9. kaido Univ 41: 1-7. Thorrington-Smith M 1970. Some new and little-known plank- Orem WH, Burnett WC, Landing WM, Lyons WB, Showers W tonic diatoms from the West Indian Ocean. Nova Hedwigia 1991. Jellyfish Lake, Palau: Early diagenesis of organic mat- Beih 64: 513-533. ter in sediments of an anoxic marine lake. Limnol Oceanogr Trigueros JM, Orive E, Arriluzea J 2002. Observations on 36: 526-543. Chaetoceros salsugineus (Chaetocerotales, Bacillariophyce- Orlova TY, Selina MS 1993. Morphology and ecology of the ae): first record of this bloom-forming diatom in a European bloom-forming planktonic diatom Chaetoceros salsugineus estuary. Eur J Phycol 37: 571-578. Takano in the Sea of Japan. Bot Mar 36: 123-130. VanLandingham SL 1968. Catalogue of the fossil and Recent Oyama K, Yoshimatsu S, Honda K, Abe Y, Fujisawa T 2005. genera and species of diatoms and their synonyms. Part II. Bloom of a large diatom Chaetoceros densus in the coastal Bacteriastrum through Coscinodiscus. Verlag von J Cramer: area of Kagawa Prefecture from Harima-Nada to Bisa-Seto, 494-1086. the Seto Inland Sea, in February 2005: environmental fea- Venkateswaran K, Shimada A, Maruyama A, Higashihara T, tures during the bloom and influence on Nori Porphyra Sakou H, Maruyama T 1993. Microbial characteristics of yezoensis cultures. Bull Jpn Soc Sci Fish 74: 660-670. [in Palau Jellyfish Lake. Can J Microbiol 39: 506-512. Japanese with English abstract] Wafar S, Untawale AG, Wafar M 1997. Litter fall and energy Paffenhöfer GA, Gardner WS 1984. Ammonium release by flux in a mangrove ecosystem. Estuar Coast Shelf Sci 44: juveniles and adult females of the subtropical marine copep- 111-124. od Eucalanus pileatus. J Plankton Res 6: 505-513. Wang X, Watkins AB 2006. Seasonal climate summary southern Pitt KA, Koop K, Rissik D 2005. Contrasting contributions to hemisphere (winter 2005): neutral conditions in the tropical inorganic nutrient recycling by the co-occurring jellyfishes, Pacific and a wet and warm winter across Australia. Aust Met Catostylus mosaicus and Phyllorhiza punctata (Scyphozoa, Mag 55: 149-160. Rhizostomeae). J Exp Mar Biol Ecol 315: 71-86. Werner D 1977. Introduction with a note on taxonomy. In Wer- Porter KG 1976. Enhancement of algal growth and productivity ner D ed, The biology of diatoms. University of California by grazing zooplankton. Science 192: 1332-1334. Press, California 13: 1-17. Proctor LM 1997. Nitrogen-fixing, photosynthetic, anaerobic Received December 28, 2009 bacteria associated with pelagic copepods. Aquat Microb Accepted August 16, 2010 Ecol 12: 105-113. Associate Editor: C Gobin

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