Pulse Perturbations from Bacterial Decomposition of Chrysaora Quinquecirrha (Scyphozoa: Pelagiidae)
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Hydrobiologia DOI 10.1007/s10750-012-1042-z JELLYFISH BLOOMS Pulse perturbations from bacterial decomposition of Chrysaora quinquecirrha (Scyphozoa: Pelagiidae) Jessica R. Frost • Charles A. Jacoby • Thomas K. Frazer • Andrew R. Zimmerman Ó Springer Science+Business Media B.V. 2012 Abstract Bacteria decomposed damaged and mor- become dominant, and cocci reproduced at a rate that ibund Chrysaora quinquecirrha Desor, 1848 releasing was 30% slower. These results, and those from a pulse of carbon and nutrients. Tissue decomposed in previous studies, suggested that natural assemblages 5–8 days, with 14 g of wet biomass exhibiting a half- may include bacteria that decompose medusae, as well life of 3 days at 22°C, which is 39 longer than as bacteria that benefit from the subsequent release of previous reports. Decomposition raised mean concen- carbon and nutrients. This experiment also indicated trations of organic carbon and nutrients above controls that proteins and other nitrogenous compounds are less by 1–2 orders of magnitude. An increase in nitrogen labile in damaged medusae than in dead or homoge- (16,117 lgl-1) occurred 24 h after increases in nized individuals. Overall, dense patches of decom- phosphorus (1,365 lgl-1) and organic carbon posing medusae represent an important, but poorly (25 mg l-1). Cocci dominated control incubations, documented, component of the trophic shunt that with no significant increase in numbers. In incubations diverts carbon and nutrients incorporated by gelati- of tissue, bacilli increased exponentially after 6 h to nous zooplankton into microbial trophic webs. Keywords Jellyfish Á Scyphomedusae Á Bacterial Guest editors: J. E. Purcell, H. Mianzan & J. R. Frost / Jellyfish decomposition Á Carbon Á Nitrogen Á Phosphorus Blooms: Interactions with Humans and Fisheries J. R. Frost (&) T. K. Frazer Institute for Hydrobiology and Fisheries Science, Fisheries and Aquatic Science Program, School of Forest University of Hamburg, Olbersweg 24, 22767 Hamburg, Resources and Conservation, University of Florida, Germany 7922 NW 71st Street, Gainesville, FL 32653, USA e-mail: [email protected] e-mail: frazer@ufl.edu Present Address: A. R. Zimmerman J. R. Frost Department of Geological Sciences, University of Florida, Fisheries and Aquatic Science Program, School of Forest 241 Williamson Hall, P.O. Box 112120, Gainesville, Resources and Conservation, University of Florida, FL 32611, USA 7922 NW 71st Street, Gainesville, FL 32653, USA e-mail: azimmer@ufl.edu C. A. Jacoby Department of Soil and Water Science, University of Florida, 7922 NW 71st Street, Gainesville, FL 32653, USA e-mail: cajacoby@ufl.edu 123 Hydrobiologia Introduction Damaged, moribund, or dead medusae should begin to decompose as they sink or drift, in part because the Medusae raise interesting questions for ecologists seek- continuous release of organic matter while they were alive ing to understand carbon and nutrient cycles in marine insures they are surrounded by a thriving bacterial systems. Individual medusae do not sequester large assemblage (Doores & Cook, 1976;Heegeretal.,1992; quantities of carbon and macronutrients because their Hansson & Norrman, 1995;Riemannetal.,2006). In bodies typically comprise 97% water and 3% organic some cases, decomposition is not completed in the water matter consisting of 72 ± 14% protein (mean ± stan- column, and carcasses of medusae carry hundreds of dard deviation), 22 ± 12% lipids, and 7 ± 5% carbo- grams of carbon to the seafloor (Miyake et al., 2002, 2005; hydrates (Larson, 1986; Schneider, 1988;Araietal., Billettetal.,2006; Koppelmann & Frost, 2008; Yamam- 1989;Clarkeetal.,1992;Lucas,1994, 2009;Doyleetal., oto et al., 2008; Murty et al., 2009). Observations of a 2007; Pitt et al., 2009). Nevertheless, dense aggregations carrion fall of Pyrosoma atlanticum Peron, 1804 (Lebrato and blooms of medusae have been recorded (Graham & Jones, 2009) suggest that benthic scavengers will feed et al., 2001; Mills, 2001;Richardsonetal.,2009), and in on accumulations of dead and moribund medusae. In such numbers, medusae irrefutably perturb the flow of addition, one set of field observations in deep water and energy and cycles of elements in an ecosystem. one set of mesocosm experiments in shallow water Mass occurrences of medusae generally last for indicate that medusae will decompose (Billett et al., 2006; weeks to months (Mills, 2001; Sexton et al., 2010), West et al., 2009). Over a period of days, bacterial and during this time, they assimilate and release decomposition and respiration created pulse perturbations carbon and nutrients creating a relatively protracted, (sensu Glasby & Underwood, 1996) consisting of press perturbation (sensu Glasby & Underwood, increased nutrients and reduced oxygen concentrations 1996). For example, medusae can consume significant as evidenced by the production of hydrogen sulfide numbers of zooplankton and larval fish and assimilate (Billett et al., 2006;Westetal.,2009). Depending on the up to 88% of the carbon in their prey (Mills, 1995; system’s response, these two perturbations could yield Arai, 1997; Purcell, 1997; Purcell & Arai, 2001; Pitt discrete or protracted responses (sensu Glasby & Under- et al., 2009). In turn, medusae excrete and secrete wood, 1996). For example, nutrients could stimulate a carbon, nitrogen, and phosphorus, primarily as mucus, discrete increase in primary productivity if there is ammonium, and phosphate (Pitt et al., 2009; Condon sufficient light, and hypoxia/anoxia could create a et al., 2011). Excretion rates vary among species, as protracted decrease in the abundance of infauna that well as with temperature and feeding history, but persists through multiple cycles of recruitment. Thus, an releases of 1,114 lmol g dry weight (DW)-1 d-1 of understanding of impacts from carrion falls of medusae dissolved organic carbon, 187 lmol g DW-1 d-1 of requires an understanding of their decomposition. ammonium, 137 lmol g DW-1 d-1 of dissolved The three previous studies that examined decom- organic nitrogen, 36 lmol g DW-1 d-1 of phosphate, position of Scyphomedusae used suffocated, frozen or and 12 lmol g DW-1 d-1 of dissolved organic phos- homogenized medusae, without controls for the phorus have been recorded (Morand et al., 1987; effects of these treatments (Titelman et al., 2006; Malej, 1989, 1991; Schneider, 1989; Nemazie et al., West et al., 2009; Tinta et al., 2010). Nevertheless, all 1993; Hansson & Norrman, 1995; Shimauchi & Uye, three studies indicate that the carcasses of scyphome- 2007; Pitt et al., 2009; Condon et al., 2010, 2011). dusae contain few refractory, structural compounds, so Rapidly accumulating evidence suggests that when they decay readily as bacteria digest their tissue, medusae reach sufficient densities, these releases thereby releasing carbon, nitrogen, and phosphorus create a press response (sensu Glasby & Underwood, (Titelman et al., 2006; West et al., 2009; Tinta et al., 1996) by supporting phytoplanktonic and bacterial 2010). Bacteria typically increased in abundance by production, although the magnitude of their influence one or more orders of magnitude over a period of days depends heavily on the availability of carbon and in incubations of suffocated or homogenized medusae nutrients from other sources and rates of flushing (Pitt (Titelman et al., 2006; Tinta et al., 2010). Measure- et al., 2005; Malej et al., 2007; Condon et al., 2010, ments of half-lives for carcasses depended on ambient 2011). Yet, what happens when the medusae in an temperatures and ranged from 0.6 to 1.0 d, but these aggregation or bloom are damaged or die? measurements potentially included unquantified loss 123 Hydrobiologia of tissue and consumption by scavengers (Titelman Materials and methods et al., 2006). In all cases, concentrations of carbon, nitrogen, and phosphorus in incubations of suffocated, Collection and handling frozen, or homogenized Scyphomedusae were signif- icantly higher than those measured in controls (Titel- Individual Scyphomedusae, Chrysaora quinquecirrha, man et al., 2006; West et al., 2009; Tinta et al., 2010). and ambient seawater were collected in 2–3 m of water This study tests hypotheses arising from the results of near the mouth of the Steinhatchee River along the three previous investigations. It employs a labora- Florida’s west coast (N 29.6°; W 83.4°). Snorkelers tory experiment to test the overall hypothesis that a pulse allowed each medusa to swim into a stationary, hand- perturbation will be created by decomposing Chrysaora held, 3-l polypropylene beaker (Kartell) that previ- quinquecirrha Desor, 1848, a scyphomedusa with a ously had been washed with a 10% hydrochloric acid circumglobal distribution and tendency to form aggre- solution to minimize contamination from beyond the gations and blooms (Graham, 2001;Grahametal., sampling site. Onboard a boat, bell diameters and any 2001; Mills, 2001;Purcell,2005; Purcell & Decker, visible signs of damage were recorded before each 2005; Hamner & Dawson, 2009;Sextonetal.,2010). In individual was placed in a new, labeled, 12-l plastic particular, the experiment addresses three related sub- bag containing ambient seawater (Table 1). Each bag hypotheses: (i) the half-life of tissue from damaged with its single medusa, was placed in a covered, 190-l medusae will be longer than 24 h, (ii) the abundance and bin containing ambient seawater. To alleviate heat composition of bacterial assemblages will differ stress, the water in the bin was replaced every 2–3 h. between incubations with