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Fecal Pellet Contents of Megalocercus Huxleyi in the Equatorial I l Biogeochemical Conditions in the Equatorial Pacific in Late 1994 New Production, Oct 15, 1994 (mmol m -2 d-1) 1O"N 6 4 O" 2 IOOS O 160"E 180" 160"W 140"W 120"W 100"W 80"W Reprinted from the Journal of Geophysical Research Published-- by the American Geophysical Union JOURNAL OF GEOPHYSICAL RESEARCH, VOL. 104, NO. C2, PAGES 3381-3390, FEBRUFY 15, 1999 Picoplankton and nanoplankton aggregation by appendicularians: Fecal pellet contents of Megalocercus lzcucleyi in the equatorial Pacific G. Gorsky,’ M. J. Chrétiennot-DinetY2J. Blaiich~t,~and I. Palazzoli’ Abstract. The content of fecal pellets of the freshly collected warm water appendicularian Megalocercus huxleyi was studied by light and electron microscopy and by flow cytometry in the superficial 100 m of the water column at 2”N, 165”E, in September 1994, during the Flux dans l’Ouest du Pacifique Equatorial (Joint Global Ocean Flux Study-France) oceanographic cruise. Microscopic observations showed that the fecal pellet contents of M lzuxteyi reflected the natural composition of the nanophytoplankton and small microphytoplankton (<50 pm). Larger cells were excluded from entering the filtering system by the inlet filters. Coccolithophorids appeared as the main component found in the feces. Evidence for ingestion of “naked” cells by this appendicularian is given. Analysis of picoplankton in fecal pellets by flow cytometer confirmed that appendicularians efficiently collect small particles. Cyanobacteria, -1 pm in diameter, were found in large quantities and showed high fluorescence in the fecal pellets. Most of these cyanobacteria in the pellets appeared to be intact, and thus may be good indicators of the appendicularian ingestion rate. The situation was different for the prochlorophyte Prochlorococcus abundant in the seawater and for picoeucaryotes (<2 pm). These were found at very low quantities in the larvacean fecal pellets. The calculations showed that with an average concentration of 5 M. huxleyi m”, >7% of the small particulate matter will be daily removed from the water. Some of this matter will be assimilated, some trapped in the houses, and the rest aggregated into rapidly sinking fecal pellets. Ingestion of large quantities of coccolithophorids indicates that appendicularians are important not only in the cycle of organic carbon but also of inorganic carbon. Moreover, if appendicularians successfully aggregate and assimilate Prochlorococcus and picoeucaryotes, then their grazing activity can represent a major pathway of carbon transformation in the tropical ecosystem 1. Introduction develop mechanisms for efficient adaptation to nutritionally dilute or to “extreme” environmental conditions. Pelagic The pelagic filter feeding tunicates, appendicularia (= tunicates are considered to be nonselective grazers, collecting larvacea), are an important component of the neritic food web. particles by sieving and also by direct interception onto filter Their importance is considered insignificant in open ocean or in fibers [Acutza et al. 19961. Appendicularians pump water oligotrophic environments. Reports made from manned through external and intemal mucous nets in extruded gelatinous submersibles in the 1960s [see Barlzain, 19791 and recent houses. Colloids >O. 1 pm and other larger particles are retained discoveries of larvacean populations adapted to aphotic oceanic and ingested [Fenaux, 1986; Flood et al.,J992]. The retention environments with low food supply contradict this view [Fenaux efficiency is determined by the pore size-Óf the internal net. It and Youngbluth, 1990; Gorsb) et al. 1991; Hainner and generally exceeds 90% for particles >3 pm [Deibel and Lee, Robison, 19921. Flood 1978, Flood et al. [1992], Deibel andLee 19921. The gut passage time of larvaceans is rapid, and fecal [1992], and Bedo et al. [1993] documented the capability of pellet production is high [Taguchi, 19821. Fecal pellets are appendicularians to shortcut the microbial food web and directly compact and ellipsoid (Figure la) and are numerous in sediment feed on submicronic particles. Hopcroft and RofS [1995] traps [Urrère and Knauer, 1981; Buck and Newton, 19951. described the rapid population growth of larvaceans in warm Megalocei-cus /zt*wleyi’s maximum trunk size can reach 5 mm, waters. These characteristics indicate that larvaceans can and the house diameter of adult specimens can reach more than 3 cm. Appendicularians feed continuously. The house secretion is ‘Observatoire OcCanologique, Université Pierre et Marie also a continuous process (the daily house production varies Curie/Centre National de la Recherche Scientifique/InstitutNational des from 1 to >IO depending on species and temperature [see Flood Sciences de l’Univers, Villefranche sur mer, France. and Deibel, 19981). Thus, because of the rapid population ’Observatoire Océanologique de Banyuls, Laboratoire Arago. Laboratoire d’océanographie Biologique, Université Pierre et Marie growth based on the short life cycle (<2 days in 29°C for Oikopleura dzoica [see Hoptcroft and Rofi 19951) and because CurieKeqtre National de la Recherche Scientifiquehstitut National des Sciences de l’Univers, Banyuls sur mer, France. of three mechanisms related to their feeding biology, (1) 3L’Institut Français de Recherche Scientifique pour le retention and ingestion of picoparticles, (2) continuous house Développement en Coopération de Nouméa, Nouméa, New Caledonia, secretion, and (3) high fecal pellet production rate, the role of France. larvaceans in the processes of aggregation can be important even Copyright 1999 by the American Geophysical Union. in weakly productive environments. Studies on the content of larvacean fecal pellets and its ‘Paper number 98JC01850. comparison with natural seston are few. The first observations 0148-0227/99/98JC-01850$9.00 of the ingested matter were made by Loknzann [1909], who 3382 GORSKY ET AL.: PICOPLANKTON AGGREGATION BY AF'PENDICULARIANS described a new size class of plankton, the nanoplankton, while from the rectdm and intestines of freshly caught adult studying the gut content of appendicularians. Alldredge [ 19771 individuals. showed in the Gulf of California that large phytoplankTon cells were off en excluded by the inlet filters from entering the house. 2.2. Light Microscopy The internal feeding filters contained diatoms and dinoflagellates in much lower proportions than in sea water. According to A subsample of fecal pellets was immediately observed with Alldredge [1977], 75%-96% of the material in the gut and in a Leitz dialux 20 microscope, equipped with a HBO 50 light fecal pellets was composed of naked flagellates and small source and a Ploemopak 2.4 vertical illuminator containing a particles. Coccolithophorids were also abundant in the gut, often 450-490 nm band path filter and exciting block (Figure lb). For in higher proportion than in seawater. Deibel and Turner [ 19851 the study of natural phytoplankton, 250 mL seawater samples studied the size of food in fecal pellets and compared it to the were filtered through 0.8 pm nuclepore membranes. A few drops pore size of the inlet filters. They also compared the size and of 37% formaldehyde (Sigma) were added during the filtration type of particles in fecal pellets with those in the environment. for cell fixation. The membrane was then placed upside down on Urban et al. [1992] described trie seasonal differences in the a slide that had been coated with a poly-L-lysine (Sigma content and composition of Oikoplezrra vanhoefeni fecal pellets Diagnostics). an adhesive solution allowing collection of in coastal Newfoundland waters. material on the slide. After removing the excess water the filter The surface waters of tropical oceanic provinces are was peeled 0% and a drop of liquid gelatin was deposited on the dominated by phytoplankton of extremely small size. In the filtered material. A coverslip was placed on the preparation and equatorial Pacific, 50%-60% of the chlorophyll biomass is was sealed when the gelatin solidtfied. Slides were kept at room contained in the 4 pm size fraction [Chavez, 1989; Le temperature in the dark and viewed onboard with the dialux or Bouteiller et al. 19921. Prochlorococcus [Chisholm et al. 1988, back at the Laboratory in Banyuls sur mer, France, with a Zeiss 19921 seems to contribute the major part of the chlorophyll of microscope, usually at x400 magnification. The content of the this fraction even in the equatorial upwelling zone [Landry et al. samples was displayed on a color Sony video system fitted to the 19961. In the western tropical Pacific, Blanchot and Roa'ier microscope and printed on a Sony video graphic printer UP-850. [1996] found the highest Proclzlorococcus concentrations in the This transfer method allowed only a semiquantitative study of superficial, oligotrophic, nitrate-depleted layer. AL hzixleyi was the natural populations and was used to compare the taxa present repeatedly found in high concentrations in the superficial in the water column and in the feces. Quantitative estimation of equatorial layer in the studied zone (Etude du Broutage en Zone diatom populations was made by scanning electron microscopy Equatoriale cruise 1996 (G. Gorsky personal observation, 1996)) (SEM) and published by Blain et al. [1997]. Other filters have and was also described in the eastern Pacific [Alldredge? 19771. been used in similar conditions, and it appears that this method In the present study we report on the content of the warm water gives a good account of the phytoplankton populations present in U hztxleyi
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