Feeding of the Estuarine Copepod Acartia Tonsa Dana ...

BULLETIN OF MARINE SCIENCE, 43(3): 458-468, 1988

FEEDING OF THE ESTUARINE COPEPOD ACARTIA TONSA DANA: CARNIVORY VS. HERBIVORY IN NATURAL MICROPLANKTON ASSEMBLAGES Dian J. Gifford and Michael J. Dagg ABSTRACT Acartia tonsa was fed natural microplankton assemblages from Terrebonne Bay, Louisiana. In experiments done under three different environmental regimes, the ratios of microzooplankton carbon: phytoplankton carbon consumed were 0.69, 0.12, and 0.03 in August, September, and January when the ratios of micro zooplankton carbon: phytoplankton carbon available were 0.03, 0.02 and 0.004 respectively. Chlorophyll was cleared at low rates « I ml·copepod-I• h-1) in the three experiments, but because of its high standing stocks (> 17 !lg' I-I) comprised a relatively large portion of the copepod's total carbon ingestion. Of the total carbon ingested, microzooplankton accounted for 41, II, and 3% in August, September, and January.

The classical paradigm of planktonic ecosystems composed of large diatoms, copepods, and fish has undergone revision during the past decade. Current understanding emphasizes the role of prokaryotes and unicellular eukaryotes, organisms of the so-called "microbial loop" (Azam et aI., 1983). The function of ciliate protozoans as trophic intermediaries between phytoplankton and copepods has been proposed by many investigators (Conover, 1964; Beers and Stewart, 1967; Pomeroy, 1974; Heinbokel and Beers, 1979; Porter et aI., 1979) and has recently received renewed attention (Sherr and Sherr, 1984; Sherr et aI., 1986). Further, negative correlations between standing stocks of protozoans and larger zooplankton may be attributed to the latter consuming the former (Smetacek, 1981; Sheldon et aI., 1986), so that predation may affect the composition, abundance and structure of microzooplankton assemblages. Although calanoid copepods are particle feeders, most studies have treated them exclusively as herbivores or carnivores. Most studies that have explicitly considered omnivory have used Artemia or other crustacean nauplii as animal prey (Anraku and Omori, 1963; Mullin, 1966; Comer et aI., 1976; Lonsdale et aI., 1979; Paffenhofer and Knowles, 1980; Landry, 1981; Conley and Turner, 1985) and have not considered the nutritional role of protozoans. Qualitatively, gut analyses show that tintinnid protozoans are ingested by calanoid copepods (Mullin, 1966; Zeitschel, 1967; Harding, 1974), and tintinnid loricae have been observed in copepod fecal pellets (Turner and Anderson, 1983). Experimental studies demonstrate that calanoid copepods ingest ciliate microzooplankton in the laboratory and in the field (Table 1).Stoecker and Sanders (1985) showed that Acartia tansa consumed both phytoplankton and tintinnid ciliates, and selected tintinnid prey when presented with a choice of equal amounts of otherwise acceptable phytoplankton food. Stoecker and Egloff(1987) made similar observations of A. tansa fed several types of planktonic ciliates and rotifers. Aloricate ciliates are generally more abundant in marine waters than the loricate tintinnids (Beers et aI., 1975; 1980). These soft bodied organisms do not possess a lorica or other hard part that would be visible in the gut or feces. In addition, they are delicate organisms that are difficult to manipulate in the laboratory (Gifford, 1985a). Consequently, their role in copepod nutrition is not well known. Terrebonne Bay, Louisiana (Fig. 1) is a highly productive coastal embayment 458

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Table 1. Cope pod ingestion of ciliates Copepod

Eurytemara affinis Acartia tansa Acartia tansa Tartanus setacaudatus Acartia hudsanica Acartia tansa Acartia clausi Acartia Acartia Acartia Acartia Acartia Acartia Acartia

clausi tansa tansa tansa tansa tansa tansa

Prey

Uronema sp. Tintinnapsis tubulasa Favella panamensis Favella panamensis Eutintinnus pectinis

Ingestion

Clearance

(ciliates-d-I)

(ml-d-')

16,800-40,800 140 80 160 288-358

99-290 107 7.2

Author

Berk, et aI., 1977 Robertson, 1983 Robertson, 1983 Robertson, 1983

Favella sp.

72-288

72-192

H elicastamella fusifarmis Favella tarakaensis Favella sp. Strabilidium sp. Strambidium sp. Tintinnapsis sp. Balanian sp. Uratricha sp.

11-69

7.4-21.5

Turner and Anderson, 1983 Stoecker and Sanders, 1985 Ayukai,1987

9.9 147 77 249-276 156 476-503 126

47.3 54 46 61-74 29-67 101-106 65

Ayukai,1987 Stoecker and Stoecker and Stoecker and Stoecker and Stoecker and Stoecker and

Egloff, 1987 Egloff, 1987 Egloff, 1987 Egloff, 1987 Egloff, 1987 Egloff, 1987

in the northern Gulf of Mexico. Typical of northern Gulf neritic waters, the bay has high standing stocks of chlorophyll throughout the year, generally > 8 ~g'l~ I (Dagg, 1984). More limited observations indicate that the size and taxonomic composition of the phytoplankton vary seasonally and that ciliate microzooplankton are abundant (Gifford, unpublished observations). Acartia tonsa is abundant in the bay, comprising a nearly monospecific stock of copepods which reproduce throughout the year (Dagg, unpublished observations). The dominant fraction of the phytoplankton in the bay is frequently < 5 ~m, too small to be captured efficiently by the congener A. clausi (Nival and Nival, 1973; 1976). Therefore, we postulated that A. tonsa in Terrebonne Bay is unable to feed efficiently on the natural phytoplankton assemblage and that ciliate protozoans may be a significant component of the diet. The purpose of our experiments was to determine what portion of the copepod's diet is composed of microzooplankton and what portion is phytoplankton. METHODS

Three experiments were done, two in late summer and one in midwinter, to assess the relative contribution of plant and animal prey to the diet of Acartia tansa under different environmental conditions (Table 2). Collections were made in Terrebonne Bay, Louisiana (Fig. I) and returned to the laboratory within 30-60 min. Copepods were collected with a 335 ,urn-mesh 0.7 5-m ring net during short (5 min) tows at z = 1 m. Seawater containing the microplankton assemblage was collected from the surface with a weighted bucket and siphoned gently through a submerged 202- ,urn mesh to remove macrozooplankton. Temperature and salinity were recorded at the time of collection. A. tansa females were sorted into ambient seawater in the laboratory. Both copepods and seawater containing the microplankton assemblage were preconditioned for 24 h at ambient temperature in darkness. The preconditioned microplankton assemblage was mixed gently and siphoned into 0.5-liter polycarbonate bottles. Twenty-five ml were removed from each bottle for chlorophyll analysis. Fifty ml were preserved with 20% (v/v) acid Iodine solution (Rodhe et aI., 1958). Fifteen Acartia tonsa females were added to each of three to five experimental bottles. Control treatments consisted of two to three bottles containing only the microplankton assemblage. All experimental and control bottles were topped up with microplankton assemblage, sealed with Parafilm without an airspace, and rotated at 0.5 rpm in darkness for 5-6 h at ambient collection temperature. Our experiments were begun in late

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BULLETIN OF MARINE SCIENCE, VOL. 43, NO.3, 1988

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Figure 1. Terrebonne Bay, Louisiana.

afternoon in order to encompass equal durations of the copepod's natural periods of daylight and darkness, thereby obviating any influence of diel rhythms on the measurement of feeding rates. At the end of each experiment, chlorophyll and microplankton samples were taken from each treatment bottle: 20-25 ml were removed for chlorophyll analysis, and 300 ml were preserved for microzooplankton enumeration. Extracted chlorophyll and phaeopigment were analyzed by fluorometry (Strickland and Parsons, 1972). Twenty-five ml subsamples of the microzooplankton were concentrated by centrifugation, with the pellet resuspended in filtered seawater in the bottom of an

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Table 2. Initial experimental conditions (values for organisms are given as number per liter)

Date

August September January

Temperature roC)

25.0 29.5 11.5

Chlorophyll a (l'g·liter-')

27.7 17.6 31.3

Tintinnids

Aloricate ciliates

Other ciliates

10 x 40 I'm Zooflagellates

1,400 540 1,090

20,360 3,160 3,360

2,380 420 3,500

18,000 2,200 0

%

Chlorophyll 20 /-Lm during a bloom oflarge diatoms. In all three experiments the microzooplankton consisted principally of ciliate protozoans, with aloricate oligotrich ciliates outnumbering tintinnids and other ciliates. During August and September, large zooflagellates (10 x 40 /-Lm) were also abundant. Ciliate abundances were high in August and lower in September and January. The diversity of the microzooplankton prey in the assemblages varied among the experiments, with seven prey categories present in August, 4 in September and 6 in January (Fig. 2). In all three experiments, most of the microzooplankton biomass was located in the larger size categories, although numerical abundance maxima tended to be located elsewhere (Fig. 2). Microzooplankton comprised 3, 2, and 0.004% of the total carbon (microzooplankton + phytoplankton) available in August, September and January respectively. A. tansa dry weights varied among the experiments, with copepods in January nearly twice the weight of those in September. Copepods were assumed to be 40% carbon. In August, A. tansa cleared 1-4 ml·copepod-l.h-I of microzooplankton and 0.10 ml·copepod-l. h-I of chlorophyll (Fig. 3A), reflecting an ingestion of 2-17 microzooplankton ·copepod-I. h-I in each size category, or a total of 62.3 microzooplankton prey·copepod-1• h-' (Fig. 3B). Normalized to carbon, this amounts to consumption of 1,224 ng microzooplankton carbon and 1,778 ng chlorophyll

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BULLETIN OF MARINE SCIENCE, VOL. 43, NO.3, 1988

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