Lethal and Sublethal Effects of Oil, Chemical Dispersant, and Dispersed Oil on the Ctenophore Mnemiopsis Leidyi

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Lethal and Sublethal Effects of Oil, Chemical Dispersant, and Dispersed Oil on the Ctenophore Mnemiopsis Leidyi Vol. 23: 237–250, 2015 AQUATIC BIOLOGY Published online April 1 doi: 10.3354/ab00625 Aquat Biol OPENPEN ACCESSCCESS Lethal and sublethal effects of oil, chemical dispersant, and dispersed oil on the ctenophore Mnemiopsis leidyi Ryan F. Peiffer, Jonathan H. Cohen* College of Earth, Ocean, and the Environment, School of Marine Science and Policy, University of Delaware, 700 Pilottown Road, Lewes, DE 19958, USA ABSTRACT: We established the lethal levels for water-accommodated fractions of Corexit® 9500A chemical dispersant, crude oil (WAF), and dispersed crude oil (CEWAF) for the ctenophore Mne- miopsis leidyi at both 15 and 23°C. This gelatinous zooplankter was sensitive to dispersant at both temperatures, as well as to oil solutions, with some increase in toxicity of CEWAF as compared to WAF. Subsequent sublethal assays for routine respiration rate, bioluminescence, and glutathione- s-transferase (GST) activity were conducted on individuals surviving 24 h exposures to test solu- tions at both 15 and 23°C. GST activity increased significantly in 2.5 and 5 mg l−1 dispersant solu- tions at 15°C, suggesting a metabolic detoxification response to the dispersant-containing solutions, but no effect of any solution type on routine respiration rate was observed. Light emis- sion through mechanically stimulated bioluminescence and photocyte lysis decreased with exposure to crude oil WAF and CEWAF at both temperatures and to dispersant exposure at 23°C. Collectively, these results demonstrate that M. leidyi exhibits both lethal and sublethal effects from acute crude oil exposure, with an elevation of some sublethal responses upon addition of chemical dispersant. Sublethal effects of oil and dispersants in pelagic species, most notably impairment of luminescence, should be considered when evaluating oil spill response strategies. KEY WORDS: Crude oil · Corexit EC9500A · Zooplankton · Glutathione-s-transferase · Respiration · Bioluminescence INTRODUCTION pelagic marine taxa. Zooplankton are important mem bers of pelagic communities, both as grazers on Accidental offshore oil releases have highlighted phytoplankton and as food for higher trophic levels the need to better understand oil and chemical dis- (Banse 1995). They are particularly susceptible to oil persant effects on pelagic organisms (Thibodeaux et and dispersant exposure given their limited ability to al. 2011, Barron 2012). In coastal areas, dispersants move away from contaminated areas as compared to are often employed to degrade surface slicks in the nekton; while some of the more mobile zooplankton interest of protecting shorelines, but their use in- species exhibit oil avoidance swimming behaviors creases exposure of pelagic organisms by allowing under laboratory conditions (Seuront 2010), the oil at the ocean surface to mix into the water column scales of large spills inevitably result in the wide- inhabited by these organisms (Reed et al. 2004). Both spread exposure of planktonic organisms (Mitra et al. lethal and sublethal toxicological data are limited for 2012). Toxicological responses of zooplankton to oil crude oil, dispersed oil, and dispersant itself across and dispersants have largely been examined in crus- a range of ecologically important and abundant taceans (e.g. Cowles & Remillard 1983a,b, Hemmer © The authors 2015. Open Access under Creative Commons by *Corresponding author: [email protected] Attribution Licence. Use, distribution and reproduction are un - restricted. Authors and original publication must be credited. Publisher: Inter-Research · www.int-res.com 238 Aquat Biol 23: 237–250, 2015 et al. 2011, Almeda et al. 2013b, Cohen et al. 2014). brates, including some zooplankton taxa, include Recently, Almeda et al. (2013a) exposed several spe- altered reproduction and settlement (Singer et al. cies of gelatinous zooplankters to crude oil emul sions. 1998, Suderman & Marcus 2002, Hjorth & Nielsen Their results suggest that gelatinous zooplankters, 2011, Villanueva et al. 2011, Goodbody-Gringley et particularly coastal ctenophores, have the potential al. 2013), respiration rate (Laughlin & Neff 1981, to be vectors of hydrocarbons up pelagic food webs, Smith & Hargreaves 1984), growth (Laughlin & Neff as these organisms survive oil exposures better than 1981), feeding (Cowles & Remillard 1983a), and loco- most zooplankton and accumulate high-molecular- motion (Cowles & Remillard 1983b, Wu et al. 1997, weight polycyclic aromatic hydrocarbons (PAHs). Seuront 2011, Cohen et al. 2014). Sublethal studies of Yet, major uncertainties remain concerning lethal enzyme activity, including glutathione-s-transferases effects of dispersed oil on gelatinous zooplankton, as (GSTs), also suggest cellular detoxification pathways well as oil/dispersant effects on sublethal physio - in zooplankton can be upregulated with hydrocarbon logical processes in these organisms. exposure (Lee 1988, Hansen et al. 2008). In gelati- Ctenophores are important links in marine food nous zooplankton, sublethal effects studies upon webs, serving as both predators of other zooplankton oil/dispersant exposure have been limited to feeding and prey for higher trophic levels including seabirds activity and swimming speed (Lee et al. 2012, and turtles (Arai 2005, Cardona et al. 2012). The Almeda et al. 2013a). Effects of oil/dispersant expo- heavy predation of adult ctenophores on other zoo- sure on bioluminescence, a key physiological prop- plankton (Granhag et al. 2011), including the larvae erty of the ctenophore M. leidyi and many other of commercially valuable fish and shellfish spe - pelagic species (reviewed in Haddock et al. 2010), cies, affects not only the populations on which they have not been investigated. Ctenophores achieve feed directly but also secondarily on phytoplankton luminescence by the oxidation of coelenterazine communities (Deason & Smayda 1982). The lobate through species-specific, calcium-dependent, oxygen- ctenophore Mnemiopsis leidyi in particular has been independent photoproteins located within special- shown to function as an important predator in coastal ized photocyte cells (Ward & Seliger 1974b, Shimo- ecosystems throughout its native range along the mura 2006). This bioluminescence most likely func tions Atlantic coast of North and South America and in the as a predator deterrent, whereby luminescent flashes Gulf of Mexico (Kremer 1994, Bayha et al. 2015). misdirect or startle a potential predator (Morin 1983, Additionally, the clearance rate on autotrophic and Haddock et al. 2010), and ctenophore luminescence heterotrophic microzooplankton by larval and post- has in turn shaped the predator-avoidance behaviors larval ctenophores is sufficiently high as to impact of their copepod prey (reviewed in Buskey et al. the base of coastal food webs during these early life 2012). For M. leidyi, the photoprotein (=mnemiopsin) stages (Stoecker et al. 1987). As ctenophore tissue is is contained in photocytes localized along meridio - relatively unprotected and exposed to surrounding nal canals; luminescence likely propagates via nu - seawater, ctenophores are potentially more suscepti- merous gap junctions after being initiated at periph- ble to the toxic effects of dispersant and dispersed oil eral nerve terminals (Anctil 1985). Mnemiopsin as compared to model fish and crustacean species, ac tivity in M. leidyi is potentially susceptible to given the tendency of chemical dispersants to de - chemical dispersants, whose membrane disruption grade biological membranes (Abel 1974). Seasonal properties may interfere with the animal’s ability to blooms of M. leidyi also create the potential for the regulate calcium in the mnemiopsin-containing exposure of large numbers of animals in the case of a photocytes. release that coincides with a bloom event (Sullivan et The present study examined lethal levels of expo- al. 2001). While Almeda et al. (2013a) studied oil- sure for a mid-Atlantic population of the ctenophore induced mortality and PAH accumulation in M. lei- M. leidyi at 2 seasonally relevant temperatures dyi, data are lacking for exposures to either disper- upon acute exposure to Corexit 9500A dispersant, sant or dispersed oil, which are relevant to coastal crude oil (WAF), and dispersed crude oil (CEWAF) spills and mitigation scenarios. to set exposure levels for sublethal experiments. Mortality following acute exposure is the most Subsequent sublethal exposure studies examining obvious detrimental effect of oil and dispersant, but parameters that may change over acute exposure sublethal toxic effects also have the potential to cre- time frames determined ctenophore respiration rate ate lasting ecological consequences (i.e. ‘ecological and capacity for bioluminescence, as well as ac - death’ sensu Singer et al. 1998). Sublethal effects of tivity of the detoxification enzyme GST in cteno - hydrocarbons and chemical dispersants on inverte- phore tissue. Peiffer & Cohen: Oil and dispersant effects in ctenophores 239 MATERIALS AND METHODS 30 mg dispersant l−1), crude oil alone (WAF, 0 to 150 mg oil l−1), or crude oil and dispersant in a 10:1 Specimen collection and laboratory acclimation ratio (CEWAF, 0 to 30 mg oil l−1) was added by gas- tight syringe. Mixing of stoppered bottles in darkness Ctenophores were collected by 15 to 30 min sets of was maintained for 18 h, followed by 4 to 6 h of a plankton net (0.75 m, 335 µm mesh) during daytime settling before drawing test solutions from the bot- flood tides from a stationary davit on a dock in the tom of the flasks for immediate
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