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Full Text in Pdf Format I MARINE ECOLOGY PROGRESS SERIES Vol. 193: 15-84, 2000 Published February 28 Mar Ecol Prog Ser Copepod grazing in a subtropical bay: species-specific responses to a midsummer increase in nanoplankton standing stock Albert Calbet*, Michael R. Landry, Rebecca D. Scheinberg Department of Oceanography, University of Hawaii at Manoa, 1000 Pope Road, Honolulu, Hawaii 96822, USA ABSTRACT: Ingestion rates of 4 small copepod species (Oithona simplex, 0. nana. Acrocalanus inermis and Parvocalanus crassirostris) were investigated in Kaneohe Bay, Hawaii, during a nudsummer increase of the pico- and nanoplankton communities. There was no evidence that adult female cope- pods fed significantly on picoplankton-sized cells. However, all the species responded behaviorally to variations in the concentration (10 to 110 pg C 1-l) and size spectrum (relative increase of cells >5 pm) of nanoplankton prey. The copepods generally behaved as opportunistic particle feeders, demonstrat- ing higher consumption rates on the most abundant cells (2-5 pm nanoplankton);however, autotrophs were usually selected over heterotrophs of simdar size. Max~murningestion rates were similar for the 2 calanoids and 0. nana (around 120000 cells copepod-' d-') and lower for 0. simplex (around 40000 cells copepod-' d-l), but biomass-specific rates of 0. simplex equaled those of the other species. At the highest nanoplankton concentrations, the ingestion rates of copepods appeared saturated, daily rations ranging from 100% body C d-' for A, rnermis to 260% body C d-l for P crassirostris. The differ- ences between ingestion rates measured as cells per copepod per day and those converted to carbon suggested that ingestion might be held below potential by the cumulahve handLing times of individual prey rather than the physioloqcal constraints of food consumption and digestive processing. KEY WORDS: Copepod . Ingestion rates . Nanoplankton . Oithona simplex . 0. nana . Acrocalanus inermis . Parvocalanus crassirostns INTRODUCTION has begun to be remedied in recent studies (Sabatini & knrboe 1994, Roff et al. 1995, Uye & Sano 1998, Marine planktonic communities comprise a wide Hopcroft & Roff 1998, Hopcroft et al. 1998),there is still variety of organisms from prokaryotes to complex relatively little known about the trophic function of metazoans. Among the latter, copepods are the most small copepods in marine ecosystems. abundant and ubiquitous group (Humes 1994, Verity & Small copepod species, along with juvenile stages of Smetacek 1996),playing important roles in the transfer larger forms, are important as trophic intermediaries of matter and energy from primary producers to hlgher between classical and microbial food webs (Roff et al. trophic levels (fish larvae) and in the export of organic 1995, Wickham 1995). This role may be specially sig- matter from the euphotic to deeper layers of the nificant in oligotrophic ecosystems, where pico-sized oceans. Most experimental research on copepods has (0.2 to 2 pm) auto- and heterotrophic organisms com- focused on larger species, and routine sampling with prise much of the system biomass (Campbell et al. relatively coarse mesh nets typically means that 1994, 1997).On average, copepods feed on prey about smaller species are undersampled or ignored in marine a factor of 18 smaller than their linear body dimensions systems (Hopcroft et al. 1998). Although this situation (Hansen et al. 1994). Therefore, smaller copepods are closer than larger copepods to the base of the microbial 'Present address: Institut de Ciencies del Mar, CSIC, Dept. food web in terms of physical constraints on their feed- Blologia Marina i Oceanografia, PS. Joan de Borbo s/n, 08039 ing mechanisms. Small copepods may also increase Barcelona, Catalunya, Spain. E-mail: [email protected] the efficiency of trophic transfer by short-circuiting O Inter-Research 2000 Resale of full article not permitted Mar Ecol Prog Ser 193: 75-84.2000 intermediate levels of protistan predators which tend calanus inermis, 508 pm & 1.0 SE; and, in Expts 3 and to feed on prey much closer to their own body size 4, Parvocalanus crassirostris, 384 pm i 0.1 SE) were (Hansen et al. 1994). added to 250 m1 polystyrene culture flasks (Corning) In the present study, we examine the feeding of filled with bay water prescreened by gentle reverse small copepods on the ambient nanoplankton commu- filtration through a 64 p mesh in order to remove nity of a subtropical embayment. In order to contribute copepods and other large grazers. These copepod con- to a better understanding of the biology and behavior centrations were higher than those in the ambient en- of small copepods in general, we compare experimen- vironment, but within the range that elicits no crowd- tal results for 4 species: 2 cyclopoids (Oithona sirnplex ing effect for the largest species, A. inermis (Kimmerer and 0. nana) and 2 calanoids (Acrocalanus inermis and 1984a). Each experiment was prepared with 4 repli- Parvocalanus crassirostns). cate treatment bottles for each species, 4 initials and 4 control bottles without added copepods. Experimental bottles were incubated in situ at 2 m MATERIALS AND METHODS depth for 24 h, the water temperature varying from 26 to 27.5"C during the study. At the beginning and end Experiments were conducted during summer and of each incubation, the water was subsampled for early autumn 1998 (Table 1) at a fixed station assessment of the pico- and nanoplankton communi- (21°25.?28'N, 157"46.713'W) in the southern basin of ties. For picoplankton abundances, 2 m1 samples were Kaneohe Bay, Oahu, Hawaii, USA. Water was col- preserved with paraformaldehyde (0.2% final concen- lected at 2 m intervals through the 12 m water column tration) and stored at -85OC (Vaulot et al. 1989). The with a 2 1Niskin bottle and gently mixed in a 20 1 poly- samples were thawed and stained with Hoeschst carbonate carboy. The abundance of copepods was 33342 (1 pg m]-') according to Monger & Landry (1993) assessed using a 0.5 m diameter plankton net with and processed using a Coulter EPIC 753 flow cyto- 64 pm mesh hauled vertically from near the bottom to meter equipped with two 5 W Argon lasers, MSDS the surface. Samples were quickly preserved in volume-control sampling and Cytomation CICERO buffered formalin (4% final concentration) for later software (Campbell et al. 1997). For nanoplankton con- study. In the laboratory, the species composition of the centrations (defined for this work as >2 pm protozoans, copepod community was estimated by counting and mostly flagellates, that passed through a 64 pm mesh), identifying at least 250 ind. sample-'. 50 m1 samples were preserved with alkaline Lugol's Experimental organisms were also collected by ver- fixative (0.005% final concentration), followed by the tical net tows, and the contents of the cod end were addition of borate-buffered formalin (2% final concen- poured into an isothermic container. The animals were tration) and sodium thiosulfate (0.3 % final concentra- transported to the laboratory within 30 min of collec- tion) (Sherr & Sherr 1993). After fixation, the samples tion and sorted under a dissecting microscope. De- were stained momentarily with proflavin (10 pg ml-' pending on the size of the copepods, 12 to 20 adult final concentration) followed by DAPI (2 pg ml-') and females of the most abundant species (Oithona sim- filtered onto 2 pm black polycarbonate membrane fil- plex, 247 pm a 0.3 SE; 0. nana, 364 pm * 2.5 SE; Acro- ters. The filters were mounted on slides with immer- Table 1 Initial abundances and net growth rates in controls (n = 4) after 24 h incubations for the different components of the nanoplankton community. Values are expressed as mean * SE. Het: heterotrophs; Auto. autotrophs 1998 2-5 pm Het 2-5 pm Auto >5 ~.lmHet >5 pm Auto Total Expt 1 (25 Jun) Cells rnl-' 3110 t 102 1150 + 223 107 r4 62 * 3 4430 pg C 1-' 5.7 1.8 1.9 2.5 12.0 Growth rate (d-l) 0.26 * 0.141 -0.31 -+ 0.226 0.34 * 0.081 -0.18 * 0.129 Expt 2 (29 Jul) Cells ml-' pg C 1-' Growth rate (d-l) Expt 3 (26 Aug] Cells ml'' pg C 1- ' Growth rate (d-l) Expt 4 (8 Oct) Cells ml- ' 9870 * 840 4500 * 870 1740 * 622 1610 i 153 17720 pg C I-' 20.0 11.0 38.0 37.0 110.0 Growth rate I&') 0.28 2 0.139 0.95 i 0.113 -0 002 i 0.356 0.97 i 0.041 Calbet et al.: Copepod grazing in a subtropical bay 7 7 sion oil and analyzed with a color image-analysis were converted to cell carbon using a factor of 0.22 pg system consisting of a Zeiss epifluorescence micro- C pm-3 (Borsheim & Bratbak 1987). Copepod carbon scope with a ZVS 3-chip CCD video camera connected contents (C) were estimated from the dry weight (DW) to a computer. The images were processed using Zeiss to length regressions of Hopcroft et al. (1998) and a Image Pro Plus software to facilitate counting and siz- C/DW ratio of 0.45 (Omori & Ikeda 1984). Selective ing of all heterotrophic and autotrophic organisms. feeding among the different nanoplankton compo- Approximately 300 individuals were enumerated and nents was calculated according to Vanderploeg & sized for each sample. We present the results in 2 size Scavia's (1979a,b) electivity index (E'): fractions; heterotrophs and autotrophs between 2 and Wi - (lIn) 5 pm (hereafter called 2-5 pm Het and 2-5 pm Auto, E,' = respectively) and cells larger than 5 pm (>5 pm Het W, + (l/n) and >5 pm Auto). where n is the number of kinds of food items and W, is Ingestion rates were calculated according to the defined by the equation: equations of Frost (1972).
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