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Obe2005a.Pdf Journal of Experimental Marine Biology and Ecology 323 (2005) 100–117 www.elsevier.com/locate/jembe Response of oxidative stress parameters and sunscreening compounds in Arctic amphipods during experimental exposure to maximal natural UVB radiation B. Obermu¨llera, U. Karstenb, D. Abelea,* aAlfred-Wegener–Institute for Polar and Marine Research, Animal Ecophysiology, Am Handelshafen 12, 27570 Bremerhaven, Germany bDepartment of Biological Sciences, Applied Ecology, University of Rostock, Albert-Einstein-Strasse 3, 18057 Rostock, Germany Received 29 October 2004; received in revised form 19 February 2005; accepted 22 March 2005 Abstract The paper investigates tolerance to UV radiation (UVR) in 3 amphipod species from the Arctic Kongsfjord, Spitsbergen: the herbivore Gammarellus homari (0- to 5-m water depth), the strictly carnivore scavenger Anonyx nugax (2- to 5-m water depth) and the detritivore/carnivore Onisimus edwardsi (2- to 5-m water depth). In previous radiation exposure experiments, both carnivore species displayed elevated mortality rates already at moderate UVR levels. Therefore, the concentrations of sunscreening compounds (mycosporine-like amino acids, MAAs, and carotenoids) and two antioxidant enzymes (superoxide dismutase, catalase) were studied in the animals under control conditions and following moderate as well as high UVR exposure. In both carnivore amphipods elevated sensitivity to experimental UVR exposure went along with a degradation of the tissue carotenoid and MAAs and a decrease of the enzymatic antioxidant defence, which resulted in increased lipid peroxidation in exposed animals. In contrast, the herbivore G. homari seems well protected by high concentrations of MAAs absorbed from its algal diet, and no oxidative stress occurred under experimental UVR. The species-specific degree of UV tolerance correlates well with the animals’ typical vertical distribution in the water column. D 2005 Elsevier B.V. All rights reserved. Keywords: Amphipods; MAAs; Oxidative stress; Polar coastal ecosystems; UVB 1. Introduction water solar irradiation, absent throughout polar winters and rapidly increasing after sea ice break-up Arctic coastal ecosystems experience strong seaso- in spring, plays a fundamental role in water column nal changes of day length and light climate. Under- processes (Williamson et al., 1994) and affects com- munity structure and productivity of benthic macro- * Corresponding author. Tel.: +49 471 4831 1567. algal assemblages and associated animals (Wiencke et E-mail address: [email protected] (D. Abele). al., 2000; Hoyer, 2003). 0022-0981/$ - see front matter D 2005 Elsevier B.V. All rights reserved. doi:10.1016/j.jembe.2005.03.005 B. Obermu¨ller et al. / J. Exp. Mar. Biol. Ecol. 323 (2005) 100–117 101 Northern high latitude shallow water ecosystems defence mechanisms scavenge ROS before critical are currently threatened by a selective increase in concentrations build up and thus establish a balance ambient UVB radiation (280–320 nm) due to ozone between pro-oxidant and antioxidant processes. depletion (Madronich et al., 1998). Although highly Among other enzymes, superoxide dismutase (SOD), S variable, Arctic total column ozone losses in winter/ converting O2À to H2O2, and catalase (CAT), convert- spring 1997–2001 amounted to 25% relative to 1980 ing H2O2 to water, represent a strong enzymatic means, peaking at 70% ozone reduction in 1999/2000 defence system (Boveris, 1998; Viarengo et al., (Executive Summary of the UNEP/WMO, 2002). This 1998). Other small molecule ROS scavengers (vita- corresponds to an estimated increase in erythermal mins C, E, h-carotene, glutathione and other redox irradiation of up to 40% at the earth’s surface. Biolo- active thiols) function as free-radical chain braking I gically relevant UVB doses reach subtidal shallow agents and singlet oxygen ( O2) quenchers. h-Caro- water depths in Northern mid- and high latitudes, tene and other carotenoids have photo-protective func- and 1% depth of surface UVB was located at 9 m in tions by absorbing energy of excited reaction products Arctic coastal areas (Bischof et al., 1998). This is still of visible and UV-light (Halliwell and Gutteridge, low compared to offshore North Atlantic waters, 1999; Montenegro et al., 2002). where 10 times more surface UVB penetrates to the Further, sunscreening compounds such as mycos- same depths (Wa¨ngberg et al., 1996; Bischof et al., porine-like amino acids (MAAs) absorb UV-photons 1998). For the Arctic Kongsfjord, Hanelt et al. (2001) and are widely distributed among aquatic organisms showed that UV radiation was high enough under (Karentz, 2001; McClintock and Karentz, 1997). They clear spring conditions to affect macroalgal primary efficiently absorb UVR in the range between 309 and productivity already in 5–6 m depth and, moreover, to 360 nm and dissipate the energy thermally without cause DNA damage already in 1–3 m depth on sum- showing fluorescence or generating oxygen radicals mer days with low water transparency (measured with (Shick and Dunlap, 2002). In addition, mycosporine– a biological dosimeter). UVB radiation can have glycine, the dominant MAA in various marine organ- direct deleterious effects in marine animals and isms, is also ascribed a moderate antioxidant potential damage biomolecules such as nucleic acids and pro- (Dunlap and Yamamoto, 1995). Pigmentation is a teins, which absorb in the UV-range. Physiological foremost protection against harmful radiation, but as disorder and death in response to direct UVB expo- shown by melanin pigmented and transparent Daph- sure were reported for northern anchovy populations nia coexisting in clear water lakes, does not uniquely (Hunter et al., 1979), northern temperate zooplankton render the animal UV-resistant (Borgeraas and Hes- and ichthyoplankton (Browman et al., 2000), tempe- sen, 2002). By its increasing effect on UVB surface rate Cladoceran Daphnia (Williamson et al., 2001), as radiation, ozone depletion has become a major envir- well as for Patagonian crustaceans (Helbling et al., onmental stressor, and UVB-induced effects are con- 2002). tributing synergistically with other environmental UVB radiation further induces generation of reac- hazards (e.g., chemical contamination, rising tempera- tive oxygen species (ROS) in surface waters. Here ture and CO2 levels) to oxidative stress conditions and hydrogen peroxide (H2O2) forms and accumulates in damage of key biomolecules in transparent marine temperate and polar regions as a consequence of DOC organisms (Livingstone, 2001; Ha¨der et al., 1995). photo-activation (Abele-Oeschger et al., 1997a; Abele Amphipods are abundant and widely distributed et al., 1999). Uncharged H2O2 passes soft body crustaceans in Arctic and subarctic regions (Jazd- surfaces by diffusion and can cause depression of zewski et al., 1995; Legezynska et al., 2000; Polter- respiration and filtration rates in invertebrates. Further, mann, 2001; Weslawski and Legezynska, 2002). H2O2 induces formation of highly reactive hydroxyl Herbivorous amphipods are associated with the rich radicals (OH.) that induce oxidative damage within macroalgal communities (Hop et al., 2002). Carnivor- cells and tissues and induce lipid peroxidation chain ous and omnivorous amphipods form an important reactions (Abele-Oeschger et al., 1997b; Abele et al., food web link between small zooplankton and detritic 1998; Abele and Puntarulo, 2004 for review). Under material and the higher trophic levels (Falk-Petersen non-stressed conditions, well-developed antioxidant et al., 1988; Hop et al., 2002 and references therein). 102 B. Obermu¨ller et al. / J. Exp. Mar. Biol. Ecol. 323 (2005) 100–117 Amphipod crustaceans are UV-transparent (Obermu¨l- colour. Despite these differences, all amphipods were ler and Abele, 2004) and intertidal species are prone to more intensely coloured on the dorsal compared to suffer stress as the irradiation climate changes. less exposed ventral side. A. nugax and O. edwardsi Further, cell membranes of polar amphipods are rich were collected at 2–5 m depth with baited traps at in polyunsaturated fatty acids (PUFA) (Graeve et al., London, a sampling site on the southern side of the 1997; Nelson et al., 2001) as an adaptation to life in island Blomstrandhalvøya (central Kongsfjord), cold climates (Clarke et al., 1985; Storelli et al., where macroalgae are restricted to single drop stones 1998). These homeoviscous adaptations render the and boulders. All A. nugax specimens exhibited a animals even more susceptible to UV-mediated oxida- similar and more uniform colouration in the range of tive damage and lipid peroxidation chain reactions milky yellow to light orange, the back being darker (Abele and Puntarulo, 2004). compared than the ventral side. The pigmentation of We investigated potentially damaging direct and O. edwardsi was bright orange to light brown, more ROS-mediated effects of UVB on three abundant intense than in A. nugax but equally uniform through- amphipod species from shallow water depths of the out collected specimens and also darker on the dorsal Kongsfjord (Spitsbergen). Irradiation experiments side. A. nugax is considered to be strictly carnivore/ were carried out simulating natural UVB doses, necrophage and able to consume large quantities of and concentrations of MAAs, as well as tissue anti- bait efficiently in short times. Whereas O. edwardsi oxidant potential and lipid peroxidation were inves- exhibits more generalistic feeding habits and is also tigated. The study forms
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