Ecology of phytoplankton communities dominated by Aureococcus anophagefferens: the role of viruses, nutrients, and microzooplankton grazing

Gobler, Christopher J.; Deonarine, Sarah; Leigh-Bell, Justine; Gastrich, Mary Downes; Anderson, O. Roger; Wilhelm, Steven W.

doi:10.1016/j.hal.2004.06.013

Cited by 47 publications

(31 citation statements)

References 39 publications

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“…As such, some have speculated that A. anophagefferens is an expatriate ocean species, which was introduced into estuaries that now host blooms (Bidigare 1989, Yentsch et al 1989, Popels et al 2003, perhaps by anthropogenic means (Doblin et al 2004). Were this the case, such an invasive species, which is not palatable by many benthic and pelagic grazers (as reviewed by Gobler et al 2005), would be expected to bloom with minimal predation loses, as was observed formally in NY (Gobler et al 2002) and currently in MD (present study), so long as the prevailing nutrient regime was favorable for this species (high levels of dissolved organic nitrogen; Gobler et al 2002Gobler et al , 2004Gobler et al , 2005. Since studies of individual protozoan grazers have shown that some species are adversely affected by A. anophagefferens, while others can consume this species (Caron et al 1989(Caron et al , 2004, consecutive blooms in the field would be expected to alter zooplankton community composition, with Aureococcus-tolerant species thriving and those adversely affected becoming less prolific.…”

mentioning

confidence: 56%

Role of zooplankton in the onset and demise of harmful brown tide blooms (Aureococcus anophagefferens) in US mid-Atlantic estuaries

Deonarine¹,

Gobler

Lonsdale³

et al. 2006

Aquat. Microb. Ecol.

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Harmful brown tides caused by the pelagophyte Aureococcus anophagefferens have occurred in mid-Atlantic estuaries for 2 decades. Low grazing rates by microzooplankton have been implicated as a possible cause of these events, but no study to date has concurrently quantified zooplankton population densities and zooplankton grazing rates of A. anophagefferens cells. We conducted field studies from 2002 to 2004 to quantify grazing on the brown tide alga A. anophagefferens by meso-, micro-, and nanozooplankton, while concurrently establishing the composition of the plankton community. Research sites included an estuary that experienced an intense brown tide (Chincoteague Bay, Maryland [MD]; 2004: 2 × 10 6 cells ml ). The MD site was dominated by small autotrophs (< 5 µm), such as A. anophagefferens and other picoeukaryotes, and small heterotrophs, such as Paulinella ovalis, while the NY site hosted a range of large and small autotrophs and zooplankton. Experiments indicated that small zooplankton (3 to 5 µm) were consumers of A. anophagefferens at bloom and non-bloom locations. However, dilution experiments documented active grazing on most picoplankton except A. anophagefferens in MD, while grazing rates on the brown tide alga in NY were comparable to grazing rates on the total phytoplankton community and other picoplankton. Experimental enrichment of estuarine waters with mesozooplankton indicated a preferential avoidance of A. anophagefferens by grazers during intense blooms, but active consumption during non-bloom conditions. Differences in the effect of grazing between sites suggest that zooplankton may be controlling brown tides in NY, but allowing blooms to form due to low grazing pressure in MD. These findings further suggest that the zooplankton community in NY has changed from one which formerly avoided the consumption of A. anophagefferens to one which currently contributes to top-down control of brown tides.KEY WORDS: Harmful algal blooms · Brown tide · Aureococcus anophagefferens · Zooplankton · Grazing · Trophic cascade · Paulinella ovalis · Synechococcus sp. Resale or republication not permitted without written consent of the publisherAquat Microb Ecol 44: [181][182][183][184][185][186][187][188][189][190][191][192][193][194][195] 2006 have negatively affected the hard clam Mercenaria mercenaria fishery as well (reviewed in Gobler et al. 2005).Aureococcus anophagefferens may adversely affect the growth and survival of micro-and mesozooplankton (Caron et al. 1989, Lonsdale et al. 1996, Sieracki et al. 2004. Microzooplankton (20 to 200 µm;Sieburth et al. 1978, Omori & Ikeda 1984 are particularly important in marine food webs as a trophic link between pico-(< 2 µm) and nanoplankton (2 to 20 µm) and mesozooplankton (> 200 µm;Lonsdale et al. 1996, Kiørboe 1998, Calbet & Landry 1999, Klein Breteler et al. 1999). During brown tides, feeding selectivity by microzooplankton may result in lower grazing rates on A. anophagefferens relative to grazing rates on co-occurring phytoplankton, thereby prom...

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confidence: 56%

Role of zooplankton in the onset and demise of harmful brown tide blooms (Aureococcus anophagefferens) in US mid-Atlantic estuaries

Deonarine¹,

Gobler

Lonsdale³

et al. 2006

Aquat. Microb. Ecol.

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“…Natural populations of A. anophagefferens appear to experience reduced grazing pressure by microbial grazers during the early phases of the development of brown tides (8,21,23). In these situations, one could expect close agreement between abundances estimated by the ELISA and IFCM methods.…”

Section: Discussionmentioning

confidence: 95%

“…In these situations, one could expect close agreement between abundances estimated by the ELISA and IFCM methods. As a bloom progresses, however, consumption by microbial predators and/or lysis by viruses may have significant impacts on the number of viable A. anophagefferens organisms in the water (8,9,17,21,23,45). These trophic interactions could significantly reduce the number of intact cells that would be observed using IFCM, but cell fragments could retain sufficient antigenic character that the ELISA method might overestimate the abundance of intact cells.…”

Section: Discussionmentioning

confidence: 99%

Immunofluorescence Flow Cytometry Technique for Enumeration of the Brown-Tide Alga, Aureococcus anophagefferens

Stauffer

Schaffner

Wazniak

et al. 2008

Appl Environ Microbiol

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A new immunologically based flow cytometry (IFCM) technique was developed to enumerate Aureococcus anophagefferens, a small pelagophyte alga that is the cause of "brown tides" in bays and estuaries of the mid-Atlantic states along the U.S. coast. The method utilizes a monoclonal antibody conjugated to fluorescein isothiocyanate (FITC-MAb) to label the surface of A. anophagefferens cells which are then detected and enumerated by using a flow cytometer. Optimal conditions for FITC-MAb staining, including solution composition, incubation times, and FITC-MAb concentrations, were determined. The FITC-MAb method was tested for cross-reactivity with nontarget, similarly sized, photoautotrophic protists, and the method was compared to an enzyme-linked immunosorbent assay (ELISA) using the same MAb. Comparisons of the IFCM technique to traditional microscopy enumeration of cultures and spiked environmental samples showed consistent agreement over several orders of magnitude (r 2 > 0.99). Comparisons of the IFCM and ELISA techniques for enumerating cells from a predation experiment showed a substantial overestimation (up to 10 times higher) of the ELISA in the presence of consumers of A. anophagefferens, presumably due to egested cell fragments that retained antigenicity, using the ELISA method, but were not characterized as whole algal cells by the IFCM method. Application of the IFCM method to environmental "brown-tide" samples taken from the coastal bays of Maryland demonstrated its efficacy in resolving A. anophagefferens abundance levels throughout the course of a bloom and over a large range of abundance values. IFCM counts of the brown-tide alga from natural samples were consistently lower than those obtained using the ELISA method and were equivalent to those of the polyclonal immunofluorescence microscopy technique, since both methods discriminate intact cells. Overall, the IFCM approach was an accurate and relatively simple technique for the rapid enumeration of A. anophagefferens in natural samples over a wide range of abundance values (10 3 to 10 6 cells ml ؊1 ).

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“…Little is known about the role of DOC uptake in augmenting autotrophic metabolisms (Lewitus 2006;Burkholder et al 2008), even though high DOC concentrations are often reported during and after blooms of algal mixotrophs (Gobler et al 2004;Mulholland et al 2009a;Boneillo and Mulholland 2014), uptake of organic N is thought to be common in the environment (Mulholland and Lomas 2008) and has been linked to algal blooms (Anderson et al 2002;Heisler et al 2008). DOM additions have been shown to stimulate algal growth; however, this growth stimulation is generally attributed to the DON (Doblin et al 1999;Fagerberg et al 2009;Loureiro et al 2009;Filippino et al 2011;Cawley et al 2013).…”

Section: Advantages Of Mixotrophymentioning

confidence: 99%

Blooms of Dinoflagellate Mixotrophs in a Lower Chesapeake Bay Tributary: Carbon and Nitrogen Uptake over Diurnal, Seasonal, and Interannual Timescales

Mulholland

Morse

Egerton

et al. 2018

Estuaries and Coasts

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A multi-year study was conducted in the eutrophic Lafayette River, a sub-tributary of the lower Chesapeake Bay during which uptake of inorganic and organic nitrogen (N) and C compounds was measured during multiple seasons and years when different dinoflagellate species were dominant. Seasonal dinoflagellate blooms included a variety of mixotrophic dinoflagellates including Heterocapsa triquetra in the late winter, Prorocentrum minimum in the spring, Akashiwo sanguinea in the early summer, and Scrippsiella trochoidea and Cochlodinium polykrikoides in late summer and fall. Results showed that no single N source fueled algal growth, rather rates of N and C uptake varied on seasonal and diurnal timescales, and within blooms as they initiated and developed. Rates of photosynthetic C uptake were low yielding low assimilation numbers during much of the study period and the ability to assimilate dissolved organic carbon augmented photosynthetic C uptake during bloom and non-bloom periods. The ability to use dissolved organic C during the day and night may allow mixotrophic bloom organisms a competitive advantage over co-occurring phytoplankton that are restricted to photoautotrophic growth, obtaining N and C during the day and in well-lit surface waters.

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Ecology of phytoplankton communities dominated by Aureococcus anophagefferens: the role of viruses, nutrients, and microzooplankton grazing

Cited by 47 publications

References 39 publications

Role of zooplankton in the onset and demise of harmful brown tide blooms (Aureococcus anophagefferens) in US mid-Atlantic estuaries

Role of zooplankton in the onset and demise of harmful brown tide blooms (Aureococcus anophagefferens) in US mid-Atlantic estuaries

Immunofluorescence Flow Cytometry Technique for Enumeration of the Brown-Tide Alga, Aureococcus anophagefferens

Blooms of Dinoflagellate Mixotrophs in a Lower Chesapeake Bay Tributary: Carbon and Nitrogen Uptake over Diurnal, Seasonal, and Interannual Timescales

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