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Growth Rates of Natural Tintinnid Populations in Narragansett Bay

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Growth Rates of Natural Tintinnid Populations in Narragansett Bay MARINE ECOLOGY PROGRESS SERIES Vol. 29: 117-126, 1986 - Published February 27 Mar. Ecol. Prog. Ser. I Growth rates of natural tintinnid populations in Narragansett Bay Peter G.Verity Graduate School of Oceanography. University of Rhode Island. Kingston, Rhode Island 02882. USA ABSTRACT: Natural microzooplankton populations were pre-screened through 202 pm mesh to remove larger predators and incubated in situ for 24 h in lower Narragansett Bay. Growth rates of tintinnid ciliates were calculated from changes in abundance; experiments were conducted at weekly intervals for 2 yr. Growth rates ranged from 0 to 3.3 doublings d-l; annual minima and maxima in growth rates occurred during the summer. Temperature regulated maximum species growth rates, while net community growth rates were primarily influenced by food quality and availability. Growth rates were depressed during blooms of small, solitary centric diatoms (Thalassiosira) and the antagonistic flagellate Olisthodiscus luteus, in agreement with previous laboratory studies. Excluding experiments when these phytoplankton were abundant, tintinnid growth rates increased asymptotic- ally with nanoplankton (< 10 pm and < 5 wm) biornass and production rates. Smaller tintinnid species showed higher maximum growth rates. Nine species exhibited maximum growth rates which equalled or exceeded 2.0 doublings d-l, and 11 other species exceeded 1.0 doubling d-l. Their high abundance and rapid growth suggest that tintinnids were important grazers of nanoplankton and rapidly entered food webs in Narragansett Bay. plankton populations while permitting water exchange with the environment, obviate these prob- One of the major problems in plankton ecology is lems and have been used successfully to measure graz- estimation of growth rates and secondary production of ing and growth rates of natural microzooplankton zooplankton. Numerous techniques have been propo- populations under in situ conditions (Stoecker et al. sed to deal with the problem of continuously breeding 1983, Verity 1986). populations, the most common being application of Tintinnids are the dominant ciliate microzooplank- laboratory-derived growth rate data to population esti- ton in lower Narragansett Bay (Verity 1984). They are mates (Uye et al. 1983), the population dynamics sufficiently abundant that small volume containers method (Durbin & Durbin 1981), and the use of such incubated in situ can be used to investigate population physiological measures as production/biomass (P/B) dynamics in the presence of their natural food supply. ratios (Tremblay & Roff 1983).Each approach is limited The present study reports on growth rates of natural by the validity of inherent assumptions and the accu- populations incubated in situ for 24 h at weekly inter- racy of basic growth variables and demographic statis- vals over a 2 yr period, and describes the functional tics (Edmondson 1974, Andrew 1983). Large volume response of growth rates to variations in temperature containment studies (Beers et al. 1977) eliminate many and phytoplankton abundance and species composi- census problems, but are expensive and labor-inten- tion. sive. The percentage of dividing cells has been propo- sed as an index of population reproduction rate of METHODS unicellular microplankton (Coats & Heinbokel 1982). However, derivation of growth rates of natural popula- Experiments were conducted in lower Narragansett tions requires knowledge of the duration of recogniz- Bay, Rhode Island (41°30'N; 71°23'W) at ca weekly able division stages for each species, which may vary intervals (n = 88) from May 1981 to July 1983. Natural with biotic and abiotic factors. Dialysis and polycarbo- microzooplankton communities were collected by nate membrane cage cultures, which contain micro- filling a 20 1 plastic bucket fitted with a 202 pm Nitex @ Inter-Research/Printed in F. R. Germany 118 Mar Ecol. Prog. Ser. mesh across the mouth to exclude larger predators. estimates. The precision of triplicate Sedgwick-Rafter Three 2 1 dialysis bags (90 mm inflated diameter, counts was k 15 % of the mean. This uncertainty was 12,000 MW cutoff), which had been autoclaved and equivalent to a maximum error of 0.2 doublings d-l. rinsed in distilled water to remove glycerin, were filled Zero growth indicated that abundance did not increase with the < 202 Km plankton communities and attached during a given experiment; declines in abundance to a mooring line at a depth of 1 m. Sample collection significantly (p < 0.05) greater than counting errors and filling of dialysis bags was conducted at the were not observed. experimental site, located 50 m offshore in 7 m of Correlations between rate and biomass parameters water. The entire process took 20 rnin, and the bags were analyzed using functional (geometric mean) were left in situ for 24 h. Incubations generally began regressions as both dependent and independent vari- between 1000 and 1200 h as preliminary experiments ables were subject to measurement error (Ricker 1973, indicated no die1 differences in tintinnid growth rates, Laws & Archie 1981). All statistical tests were per- in agreement with previous investigations (Heinbokel formed according to Snedecor & Cochran (1967). 1978b, Coats & Heinbokel 1982). Temperature dependence (T) of growth rate (K) was Chlorophyll a (chl a) and particulate organic carbon analyzed using K = exm. QIo was defined as elO(X). (POC) in the <l53 pm, <l0 pm, and <S size fractions, and tintinnid abundance were measured on subsamples from the initial community; final tintinnid RESULTS abundance in each of the 3 bags was determined after 24 h. Samples were filtered onto Gelman A/E 0.45 pm Twenty-six tintinnid species representing 9 genera glass fiber filters. Chl a was extracted in 90 % acetone were enumerated (Table 1). The genus Tintinnopsis by grinding and measured in triplicate before and after contributed the most species (ll), followed by acidification using the fluorometric method of Holm- Stenosemella (3) and Eutintinnus (2).Three Tintinnop- Hansen et al. (1965).POC was determined in duplicate sis species exhibited the highest abundance maxima: on a Hewlett Packard 185B CHN analyzer (Sharp 1974). The mean coefficient of variation of triplicate Table 1. Tintinnid species and their maximum abundance (C) chl a measurements on population subsamples was (X 103 1-l) in the dialysis bags + 4 %, and the range of duplicate POC measurements was k 8 % of the mean. Species C One 1 from the initial bucket sample and 1 1 from each of the 3 dialysis bags after 24 h were preserved in Eutintinnus pectinis (Kofoid & Campbell) 0.7 seawater-buffered formalin and concentrated by set- (= Tintinnus pectinis of Hargraves 1981) tling to a final volume of 5 to 10 ml. A minimum of 3 Eutintinnussp. (= Tintinnussp. of Hargraves 1981) 2.7 replicate 1 m1 counts in Sedgwick Rafter chambers Favella sp. (see Verity & Stoecker 1982) 0.3 Helicostomella subulata (Ehrenberg) Jorgensen 3.5 from the initial and each of the 3 final 5 to 10 m1 Metacylis annulifera (Ostenfeld & Schmidt) 2.0 concentrates assessed initial and final tintinnid abun- Parafavella sp. (see Davis 1978) 0.1 dances; entire samples were enumerated during Stenosemella oliva (Meunier) 4.0 periods of low abundance. Identification (Table 1) was Stenosernella steini (Jorgensen) 1.7 Stenosemella ventricosa 0.6 & based on lorica morphology after Kofoid Campbell (Clap. & Lachm.) Jorgensen (1929, 1939). Tintinnid growth rates (doublings d-l) Stylicauda platensis 0.1 were calculated for each dialysis bag, assuming expo- (Cunha & Fonseca) (see Cosper 1972) nential growth (Verity & Stoecker 1982), from: Tintinnidium fluviatile (Stein) Kent 1.1 Tintinnopsis acuminata Daday 9.6 Tintinnopsis baltica Brandt 1.1 Tintinnopsis beroidea Stein 1.7 where N, and No = tintinnid numbers at Days 1 and 0. Tintinnopsis dadayi Kofoid 0.1 Mean community growth rates (K) represent the mean Tintinnopsis kofoidi Hada 0.5 increase in abundance in the 3 dialysis bags of all Tintinnopsis levigata (Kofoid & Campbell) 0.4 Tintinnopsis minu ta Wailes 70.0 species combined during the 24 h incubations. Max- Tintinnopsis nucula (Fol) Brandt 0.1 imum growth rates (K,) represent the maximum Tintinnopsis parva Merkle 1.2 observed rate for an individual species averaged over Tintinnopsis rapa Meunier 3.0 the 3 dialysis bags within a given experiment. Species Tintinnopsis tubulosoides Meunier 0.5 growth rates in Table 2 represent growth rates in Tintinnopsis undella Meunier 0.2 Tintinnopsis urnula Meunier 0.2 experiments in which the final mean abundance of a Tint~nnopsisvasculum Meunier 5.0 given species exceeded 100 lY1, as lower abundances Tintlnnopsis ventncosoides Meunier 1 .O generally had broad confidence intervals around mean Verity: Growth rates of tintinnids 119 T. minuta (70.0 X 103 1-l), T. acuminata (9.6 X 103), experiments, respectively. T. minuta, Eutintinnuspec- and T. vasculum (5.0 X 103).A total of 14 of 26 species tinis, and Eutintinnus sp. grew at an average rate of 1.7 showed maximum abundances exceeding 103 tintin- to 1.8 doublings d-' in all experiments in which they nids 1-l. Species number in a given experiment ranged were present. Three common species, T. acuminata, T. from 2 to 15, and was highest during latesummer and fluviatile, and T. baltica, grew at mean rates of 0.9 to earlyfall (Fig. 1). The lowest number of tintinnid 1.1 doublings d-l; 4 rare species (Favella sp., T. species generally occurred during late fall and winter. beroidea, T. dadayi, and T. kofoidi] averaged 1 to 2 Tintinnid community growth rates ranged from 1.9 to doublings d-l. 2.4 doublings d-I during the summer of 1981, and then Chl a in the < 153 pm fraction was 4 to 5 pg 1-I declined to 0.3 doublings d-' during October. Growth during the summer of 1981 (Fig. 2), due primarily to the rates fluctuated between 0.2 and 1.0 doublings d-I dinoflagellates Katodinium rotundatum, Prorocentrum during the winter, with no growth observed in late minimum, P.
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