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Sex and microhabitat influence the uptake and allocation of mycosporine-like amino acids to tissues in the purple sea urchin, Strongylocentrotus purpuratus

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Abstract

UVR-absorbing mycosporine-like amino acids (MAAs) were detected in tissues of Strongylocentrotus purpuratus and in ten species of Rhodophyte macroalgae (eight previously untested) collected from intertidal microhabitats in November and January 2006–2007 in Central California (35°09′N, 120°45′W). In sea urchins, MAA concentrations were higher in ovaries than testes, while epidermal concentrations were similar between sexes. Ovaries and epidermal tissues had similar MAA signatures and broadband UVA/UVB absorbance, while testes had a narrower absorption ranges shifted toward higher energy wavelengths. Sea urchins occupying pits in the substrate exhibited lower MAA concentrations than those outside pits, suggesting adult microhabitat may impact UV protection. Light levels did not influence gonadal MAA concentrations, but correlated with elevated epidermal MAA concentrations for males in the sunniest microhabitat. This study suggests sex and habitat strongly influence MAA concentrations among individual S. purpuratus and that allocation of MAA sunscreens to tissues in response to UVR is sex-dependent.

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References

  • Adams NL, Shick JM (1996) Mycosporine-like amino acids provide protection against ultraviolet radiation in eggs of the green sea urchin Strongylocentrotus droebachiensis. Photochem Photobiol 64(1):149–158. doi:10.1111/j.1751-1097.1996.tb02435

    Article  CAS  Google Scholar 

  • Adams NL, Shick JM (2001) Mycosporine-like amino acids prevent UVb-induced abnormalities during early development of the green sea urchin Strongylocentrotus droebachiensis. Mar Biol 138(2):267–280. doi:10.1007/s002270000463

    Article  CAS  Google Scholar 

  • Adams NL, Shick JM, Dunlap WC (2001) Selective accumulation of mycosporine-like amino acids in ovaries of the green sea urchin Strongylocentrotus droebachiensis is not affected by ultraviolet radiation. Mar Biol 138(2):281–294. doi:10.1007/s002270000464

    Article  CAS  Google Scholar 

  • Arkle RS, Pilliod DS (2010) Prescribed fires as ecological surrogates for wildfires: a stream and riparian perspective. Forest Ecol Manag 259(5):893–903. doi:10.1016/j.foreco.2009.11.029

    Article  Google Scholar 

  • Bandaranayake WM, Des Rocher A (1999) Role of secondary metabolites and pigments in the epidermal tissues, ripe ovaries, viscera, gut contents and diet of the sea cucumber Holothuria atra. Mar Biol 133(1):163–169. doi:10.1007/s002270050455

    Article  CAS  Google Scholar 

  • Bosch I, Janes P, Schack R, Steves B, Karentz D (1994) Survey of UV-absorbing compounds in sub-tropical sea urchins from Florida and the Bahamas. Am Zool 34:102A

    Google Scholar 

  • Campanale JP, Tomanek L, Adams NL (2011) Exposure to ultraviolet radiation causes proteomic changes in embryos of the purple sea urchin, Strongylocentrotus purpuratus. J Exp Mar Biol Ecol 397:106–120. doi:10.1016/j.jembe.2010.11.022

    Article  CAS  Google Scholar 

  • Carefoot TH, Karentz D, Pennings SC, Young CL (2000) Distribution of mycosporine-like amino acids in the sea hare Aplysia dactylomela: effect of diet on amounts and types sequestered over time in tissues and spawn. Comp Biochem Physiol C 126(1):91–104. doi:10.1016/S0742-8413(00)00098-0

    Article  CAS  Google Scholar 

  • Carreto JI, Carignan MO (2011) Mycosporine-like amino acids: relevant secondary metabolites. Chemical and ecological aspects. Mar Drugs 9(3):387–446. doi:10.3390/md9030387

    Article  CAS  Google Scholar 

  • Carroll AK, Shick JM (1996) Dietary accumulation of UV-absorbing mycosporine-like amino acids (MAAs) by the green sea urchin (Strongylocentrotus droebachiensis). Mar Biol 124(4):561–569. doi:10.1007/BF00351037

    Article  CAS  Google Scholar 

  • Conde FR, Carignan MO, Churio MS, Carreto JI (2003) In vitro cis-trans photoisomerization of palythene and usujirene: implications on the in vivo transformation of mycosporine-like amino acids. Photochem Photobiol 77(2):146–150. doi:10.1562/0031-8655(2003)0770146IVCTPO2.0.CO2

    Article  CAS  Google Scholar 

  • Dayton PK (1975) Experimental evaluation of ecological dominance in a rocky intertidal algal community. Ecol Monogr 45(2):137–159. doi:10.2307/1942404

    Article  Google Scholar 

  • de la Coba F, Aguilera J, Figueroa FL, de Galvez MV, Herrera E (2009) Antioxidant activity of mycosporine-like amino acids isolated from three red macroalgae and one marine lichen. J Appl Phycol 21(2):161–169. doi:10.1007/s10811-008-9345-1

    Article  Google Scholar 

  • Denny M, Gaylord B (1996) Why the urchin lost its spines: hydrodynamic forces and survivorship in three echinoids. J Exp Biol 199(3):717–729

    Google Scholar 

  • Dunlap WC, Chalker BE (1986) Identification and quantitation of near-UV absorbing compounds S-320 in a hermatypic scleractinian. Coral Reefs 5(3):155–160. doi:10.1007/BF00298182

    Article  CAS  Google Scholar 

  • Dunlap WC, Shick JM (1998) Ultraviolet radiation-absorbing mycosporine-like amino acids in coral reef organisms: a biochemical and environmental perspective. J Phycol 34(3):418–430. doi:10.1046/j.1529-8817.1998.340418

    Article  Google Scholar 

  • Dunlap WC, Yamamoto Y (1995) Small-molecule antioxidants in marine organisms: antioxidant activity of mycosporine-glycine. Comp Biochem Physiol B 112(1):105–114. doi:10.1016/0305-0491(95)00086-N

    Article  Google Scholar 

  • Dunlap WC, Williams DM, Chalker BE, Banaszak AT (1989) Biochemical photoadaptation in vision: UV-absorbing pigments in fish eye tissues. Comp Biochem Physiol B 93(3):601–608. doi:10.1016/0305-0491(89)90383-0

    Google Scholar 

  • Ebert TA (1968) Growth rates of the sea urchin Strongylocentrotus purpuratus related to food availability and spine abrasion. Ecology 49(6):1075–1901. doi:10.2307/1934491

    Article  Google Scholar 

  • Epel D, Hemela K, Shick M, Patton C (1999) Development in the floating world: defenses of eggs and embryos against damage from UV radiation. Am Zool 39(2):271–278. doi:10.1093/icb/39.2.271

    Google Scholar 

  • Forster P, Ramaswamy V, Artaxo P, Berntsen T, Betts R, Fahey DW, Haywood J, Lean J, Lowe DC, Myhre G, Nganga J, Prinn R, Raga G, Schulz M, Van Dorland R (2007) Changes in atmospheric constituents and in radiative forcing. In: Solomon S, Qin D, Manning M, Chen Z, Marquis M, Averyt KB, Tignor M, Miller HL (eds) Climate change 2007: the physical science basis. Contribution of working group I to the fourth assessment report of the intergovernmental panel on climate change. Cambridge University Press, Cambridge

    Google Scholar 

  • Franklin LA, Forster RM (1997) The changing irradiance environment: consequences for marine macrophyte physiology, productivity and ecology. Eur J Phycol 32(3):207–232. doi:10.1080/09670269710001737149

    Google Scholar 

  • Franklin LA, Yakovleva I, Karsten U, Luning K (1999) Synthesis of mycosporine-like amino acids in Chondrus crispus (Florideophyceae) and the consequences for sensitivity to ultraviolet B radiation. J Phycol 35(4):682–693. doi:10.1080/09670269710001737149

    Article  CAS  Google Scholar 

  • Furusaki A, Matsumoto T, Tsujino I, Sekikawa I (1980) Crystal and molecular structure of palythine trihydrate. Bull Chem Soc Jpn 53(2):319–323. doi:10.1246/bcsj.53.319

    Article  CAS  Google Scholar 

  • Giese AC, Pearse JS, Pearse VB (1991) Reproduction of marine invertebrates: echinoderms and lophophorates, vol 6. Blackwell, New York

    Google Scholar 

  • Grupe BM (2006) Purple sea urchins (Stronglyocentrotus purpuratus) in and out of pits: the effects of microhabitat on population structure, morphology, growth and mortality. Master Thesis. University of Oregon, Eugene

  • Häder DP, Helbling EW, Williamson CE, Worrest RC (2011) Effects of UV radiation on aquatic ecosystems and interactions with climate change. Photochem Photobiol 10(2):242–260. doi:10.1039/c0pp90036b

    Article  Google Scholar 

  • Himmelman JH (1978) Reproductive cycle of the green sea urchin, Strongylocentrotus droebachiensis. Can J Zool 56(8):1828–1836. doi:10.1139/z78-249

    Article  Google Scholar 

  • Hoyer K, Karsten U, Wiencke C (2002) Induction of sunscreen compounds in Antarctic macroalgae by different radiation conditions. Mar Biol 141(4):619–627. doi:10.1007/s00227-002-0871-0

    Article  CAS  Google Scholar 

  • Karentz D, McEuen FS, Land MC, Dunlap WC (1991) Survey of mycosporine-like amino acid compounds in Antarctic marine organisms: potential protection from UV exposure. Mar Biol 108(1):157–166. doi:10.1007/BF01313484

    Article  CAS  Google Scholar 

  • Karentz D, Dunlap WC, Bosch I (1997) Temporal and spatial occurrence of UV-absorbing mycosporine-like amino acids in tissues of the antarctic sea urchin Sterechinus neumayeri during springtime ozone-depletion. Mar Biol 129(2):343–353. doi:10.1007/s002270050174

    Article  CAS  Google Scholar 

  • Karsten U, Sawall T, Hanelt D, Bischof K, Figueroa FL, Flores-Moya A, Wiencke C (1998) An inventory of UV-absorbing mycosporine-like amino acids in macroalgae from polar to warm-temperate regions. Bot Mar 41(5):443–453. doi:10.1515/botm.1998.41.1-6.443

    CAS  Google Scholar 

  • Karsten U, Bischof K, Hanelt D, Tug H, Wiencke C (1999) The effect of ultraviolet radiation on photosynthesis and ultraviolet-absorbing substances in the endemic Arctic macroalga Devaleraea ramentacea (Rhodophyta). Physiol Plant 105(1):58–66. doi:10.1034/j.1399-3054.1999.105110

    Article  CAS  Google Scholar 

  • Lamare MD, Hoffman J (2004) Natural variation of carotenoids in the eggs and gonads of the echinoid genus, Strongylocentrotus: implications for their role in ultraviolet radiation photoprotection. J Exp Mar Biol Ecol 312(2):215–233. doi:10.1016/j.jembe.2004.02.016

    Article  CAS  Google Scholar 

  • Lamare MD, Lesser MP, Barker MF, Barry TM, Schimanski KB (2004) Variation in sunscreen compounds (mycosporine-like amino acids) for marine species along a gradient of ultraviolet radiation transmission within Doubtful Sound, New Zealand. NZ J Mar Freshwat Res 38(5):775–793

    Article  CAS  Google Scholar 

  • Lamare MD, Barker MF, Lesser MP, Marshall C (2006) DNA photorepair in echinoid embryos: effects of temperature on repair rate in Antarctic and non-Antarctic species. J Exp Biol 209(24):5017–5028. doi:10.1242/jeb.02598

    Article  CAS  Google Scholar 

  • Lamare M, Burritt D, Lister K (2011) Ultraviolet radiation and echinoderms: past, present and future perspectives. Adv Mar Biol 59:145–187. doi:10.1016/B978-0-12-385536-7.00004-2

    Article  Google Scholar 

  • Lee TM, Shiu CT (2009) Implications of mycosporine-like amino acid and antioxidant defenses in UV-B radiation tolerance for the algae species Pterocladiella capillacea and Gelidium amansii. Mar Environ Res 67(1):8–16. doi:10.1016/j.marenvres.2008.09.006

    Article  CAS  Google Scholar 

  • Lesser MP (2010) Depth-dependent effects of ultraviolet radiation on survivorship, oxidative stress and DNA damage in sea urchin (Strongylocentrotus droebachiensis) embryos from the Gulf of Maine. Photochem Photobiol 86(2):382–388. doi:10.1111/j.1751-1097.2009.00671

    Article  CAS  Google Scholar 

  • Lesser MP, Kruse VA, Barry TM (2003) Exposure to ultraviolet radiation causes apoptosis in developing sea urchin embryos. J Exp Biol 206(22):4097–4103. doi:10.1242/jeb.00621

    Article  Google Scholar 

  • Lesser MP, Lamare MD, Barker MF (2004) Transmission of ultraviolet radiation through the Antarctic annual sea ice and its biological effects on sea urchin embryos. Limnol Oceanogr 49(6):1957–1963. doi:10.4319/lo.2004.49.6.1957

    Article  Google Scholar 

  • Lesser MP, Barry TM, Lamare MD, Barker MF (2006) Biological weighting functions for DNA damage in sea urchin embryos exposed to ultraviolet radiation. J Exp Mar Biol Ecol 328(1):10–21. doi:10.1016/j.jembe.2005.06.010

    Article  CAS  Google Scholar 

  • Levitan DR (1993) The importance of sperm limitation to the evolution of egg size in marine invertebrates. Am Nat 141(4):517–536

    Article  CAS  Google Scholar 

  • Li HW, Lamberti GA, Pearsons TN, Tait CK, Li JL, Buckhouse JC (1994) Cumulative effects of riparian disturbances along high desert trout streams of the John Day Basin, Oregon. T Am Fish Soc 123(4):627–640. doi:10.1577/1548-8659(1994)123<0627:ceorda>2.3.co;2

    Article  Google Scholar 

  • Madronich S, McKenzie RL, Bjorn LO, Caldwell MM (1998) Changes in biologically active ultraviolet radiation reaching the earth’s surface. J Photochem Photobiol B Biol 46(1–3):5–19. doi:10.1016/S1011-1344(98)00182-1

    Article  CAS  Google Scholar 

  • Mason DS, Schafer F, Shick JM, Dunlap WC (1998) Ultraviolet radiation-absorbing mycosporine-like amino acids (MAAs) are acquired from their diet by medaka fish (Oryzias latipes) but not by SKH-1 hairless mice. Comp Biochem Physiol A 120(4):587–598. doi:10.1016/S1095-6433(98)10069-7

    Article  CAS  Google Scholar 

  • McClintock JB, Karentz D (1997) Mycosporine-like amino acids in 38 species of subtidal marine organisms from McMurdo Sound, Antarctica. Antarct Sci 9(4):392–398. doi:10.1017/S0954102097000503

    Article  Google Scholar 

  • McKenzie RL, Aucamp PJ, Bais AF, Bjorn LO, Ilyas M (2007) Changes in biologically-active ultraviolet radiation reaching the earth’s surface. Photochem Photobiol Sci 6(3):218–231. doi:10.1016/S1011-1344(98)00182-1

    Article  CAS  Google Scholar 

  • Michalek-Wagner K (2001) Seasonal and sex-specific variations in levels of photo-protecting mycosporine-like amino acids (MAAs) in soft corals. Mar Biol 139(4):651–660. doi:10.1007/s002270100625

    CAS  Google Scholar 

  • Naumburg E, DeWald LE (1999) Relationships between Pinus ponderosa forest structure, light characteristics, and understory graminoid species presence and abundance. Forest Ecol Manag 124(2–3):205–215. doi:10.1016/s0378-1127(99)00067-5

    Article  Google Scholar 

  • Neale PJ, Banaszak AT, Jarriel CR (1998) Ultraviolet sunscreens in Gymnodinium sanguineum (Dinophyceae): mycosporine-like amino acids protect against inhibition of photosynthesis. J Phycol 34(6):928–938. doi:10.1046/j.1529-8817.1998.340928

    Article  CAS  Google Scholar 

  • Newman SJ, Dunlap WC, Nicol S, Ritz D (2000) Antarctic krill (Euphausia superba) acquire a UV-absorbing mycosporine-like amino acid from dietary algae. J Exp Mar Biol Ecol 255(1):93–110. doi:10.1016/S0022-0981(00)00293-8

    Article  CAS  Google Scholar 

  • Oren A, Gunde-Cimerman N (2007) Mycosporines and mycosporine-like amino acids: UV protectants or multipurpose secondary metabolites? FEMS Microbiol Lett 269(1):1–10. doi:10.1111/j.1574-6968.2007.00650

    Article  CAS  Google Scholar 

  • Pennington JT (1985) The ecology of fertilization of echinoid eggs—the consequences of sperm dilution, adult aggregation, and synchronous spawning. Biol Bull 169(2):417–430

    Article  Google Scholar 

  • Przeslawski R, Benkendorff K, Davis AR (2005) A quantitative survey of mycosporine-like amino acids (MAAs) in intertidal egg masses from temperate rocky shores. J Chem Ecol 31(10):2417–2438. doi:10.1007/s10886-005-7110-3

    Article  CAS  Google Scholar 

  • Rastogi RP, Richa SinhaRP, Singh SP, Häder DP (2010) Photoprotective compounds from marine organisms. J Ind Microbiol Biotechnol 37(6):537–558. doi:10.1007/s10295-010-0718-5

    Article  CAS  Google Scholar 

  • Sea Urchin Genome Sequencing Consortium, Sodergren E, Weinstock GM, Davidson EH, Cameron RA, Gibbs RA, Angerer RC, Angerer LM, Arnone MI, Burgess DR, Burke RD, Coffman JA, Dean M, Elphick MR, Ettensohn CA, Foltz KR, Hamdoun A, Hynes RO, Klein WH, Marzluff W, McClay DR, Morris RL, Mushegian A, Rast JP, Smith LC, Thorndyke MC, Vacquier VD, Wessel GM, Wray G, Zhang L, Elsik CG, Ermolaeva O, Hlavina W, Hofmann G, Kitts P, Landrum MJ, Mackey AJ, Maglott D, Panopoulou G, Poustka AJ, Pruitt K, Sapojnikov V, Song X, Souvorov A, Solovyev V, Wei Z, Whittaker CA, Worley K, Durbin KJ, Shen Y, Fedrigo O, Garfield D, Haygood R, Primus A, Satija R, Severson T, Gonzalez-Garay ML, Jackson AR, Milosavljevic A, Tong M, Killian CE, Livingston BT, Wilt FH, Adams N, Bellé R, Carbonneau S, Cheung R, Cormier P, Cosson B, Croce J, Fernandez-Guerra A, Genevière AM, Goel M, Kelkar H, Morales J, Mulner-Lorillon O, Robertson AJ, Goldstone JV, Cole B, Epel D, Gold B, Hahn ME, Howard-Ashby M, Scally M, Stegeman JJ, Allgood EL, Cool J, Judkins KM, McCafferty SS, Musante AM, Obar RA, Rawson AP, Rossetti BJ, Gibbons IR, Hoffman MP, Leone A, Istrail S, Materna SC, Samanta MP, Stolc V, Tongprasit W, Tu Q, Bergeron KF, Brandhorst BP, Whittle J, Berney K, Bottjer DJ, Calestani C, Peterson K, Chow E, Yuan QA, Elhaik E, Graur D, Reese JT, Bosdet I, Heesun S, Marra MA, Schein J, Anderson MK, Brockton V, Buckley KM, Cohen AH, Fugmann SD, Hibino T, Loza-Coll M, Majeske AJ, Messier C, Nair SV, Pancer Z, Terwilliger DP, Agca C, Arboleda E, Chen N, Churcher AM, Hallböök F, Humphrey GW, Idris MM, Kiyama T, Liang S, Mellott D, Mu X, Murray G, Olinski RP, Raible F, Rowe M, Taylor JS, Tessmar-Raible K, Wang D, Wilson KH, Yaguchi S, Gaasterland T, Galindo BE, Gunaratne HJ, Juliano C, Kinukawa M, Moy GW, Neill AT, Nomura M, Raisch M, Reade A, Roux MM, Song JL, Su YH, Townley IK, Voronina E, Wong JL, Amore G, Branno M, Brown ER, Cavalieri V, Duboc V, Duloquin L, Flytzanis C, Gache C, Lapraz F, Lepage T, Locascio A, Martinez P, Matassi G, Matranga V, Range R, Rizzo F, Röttinger E, Beane W, Bradham C, Byrum C, Glenn T, Hussain S, Manning G, Miranda E, Thomason R, Walton K, Wikramanayke A, Wu SY, Xu R, Brown CT, Chen L, Gray RF, Lee PY, Nam J, Oliveri P, Smith J, Muzny D, Bell S, Chacko J, Cree A, Curry S, Davis C, Dinh H, Dugan-Rocha S, Fowler J, Gill R, Hamilton C, Hernandez J, Hines S, Hume J, Jackson L, Jolivet A, Kovar C, Lee S, Lewis L, Miner G, Morgan M, Nazareth LV, Okwuonu G, Parker D, Pu LL, Thorn R, Wright R (2006) The genome of the sea urchin Strongylocentrotus purpuratus. Science 314(5801):941–952. doi:10.1126/science.1133609

  • Sekikawa I, Kubota C, Hiraoki T, Tsujino I (1986) Isolation and structure of a 357 nm UV-absorbing substance usujirene from the red alga Palmaria palmata (l. O. Kuntze). Jpn J Phycol 34(3):185–188

    CAS  Google Scholar 

  • Shick JM (2004) The continuity and intensity of ultraviolet irradiation affect the kinetics of biosynthesis, accumulation, and conversion of mycosporine-like amino acids (MAAs) in the coral Stylophora pistillata. Limnol Oceanogr 49(2):442–458

    Article  CAS  Google Scholar 

  • Shick JM, Dunlap WC (2002) Mycosporine-like amino acids and related gadusols: biosynthesis, accumulation, and UV-protective functions in aquatic organisms. Annu Rev Physiol 64:223–262. doi:10.1146/annurev.physiol.64.081501.155802

    Article  CAS  Google Scholar 

  • Shick JM, Romaine-Lioud S, Ferrier-Pages C, Gattuso JP (1999) Ultraviolet-B radiation stimulates shikimate pathway-dependent accumulation of mycosporine-like amino acids in the coral Stylophora pistillata despite decreases in its population of symbiotic dinoflagellates. Limnol Oceanogr 44(7):1667–1682

    Article  CAS  Google Scholar 

  • Sinha RP, Klisch M, Groniger A, Hader DP (1998) Ultraviolet-absorbing/screening substances in cyanobacteria, phytoplankton and macroalgae. J Photochem Photobiol B Biol 47(2–3):83–94. doi:10.1016/s1011-1344(98)00198-5

    Article  CAS  Google Scholar 

  • Sinha RP, Singh SP, Häder DP (2007) Database on mycosporines and mycosporine-like amino acids (MAAs) in fungi, cyanobacteria, macroalgae, phytoplankton and animals. J Photochem Photobiol B Biol 89(1):29–35. doi:10.1016/j.jphotobiol.2007.07.006

    Article  CAS  Google Scholar 

  • Strathmann MF (1987) Reproduction and development of marine invertebrates of the northern Pacific Coast: data and methods for the study of eggs, embryos, and larvae. University of Washington Press, Seattle

    Google Scholar 

  • Tedetti M, Sempere R (2006) Penetration of ultraviolet radiation in the marine environment, a review. Photochem Photobiol 82(2):389–397. doi:10.1562/2005-11-09-IR-733

    Article  CAS  Google Scholar 

  • Vadas RL (1968) The ecology of Agarum and the kelp bed community. Dissertation. Univeristy of Washington, Seattle

  • van de Poll WH, Hanelt D, Hoyer K, Buma AGJ, Breeman AM (2002) Ultraviolet-B-induced cyclobutane-pyrimidine dimer formation and repair in arctic marine macrophytes. Photochem Photobiol 76(5):493–500. doi:10.1562/0031-8655(2002)0760493UBICPD2.0.CO2

    Article  Google Scholar 

  • Walker C, Tatsuya U, Lesser M (2007) Gametogenesis and reproduction of sea urchins. In: Lawrence J (ed) Edible sea urchins: biology and ecology, vol 1. Elsevier, Amsterdam, p 24

    Google Scholar 

  • Whitehead K, Karentz D, Hedges JI (2001) Mycosporine-like amino acids (MAAs) in phytoplankton, a herbivorous pteropod (Limacina helicina), and its pteropod predator (Clione antarctica) in McMurdo Bay, Antarctica. Mar Biol 139(5):1013–1019. doi:10.1007/s002270100654

    Article  CAS  Google Scholar 

  • Zepp RG, Erickson DJ, Paul ND, Sulzberger B (2011) Effects of solar uv radiation and climate change on biogeochemical cycling: interactions and feedbacks. Photochem Photobiol Sci 10(2):261–279. doi:10.1039/c0pp90037k

    Article  CAS  Google Scholar 

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Acknowledgments

We thank many volunteers on this project especially L. Chang, M. Daugherty, J. Campanale, A. Lydon, J. Kershner, B. Brown and T. Moylan. Thanks to M. Moline, S. Morgan and S. Miller for guidance on the project and manuscript and J. W. White, J. Sklar, and S. Rein for help with statistical analyses. We appreciate the generosity of W. Dunlap for providing MAA standards, D. Pilliod and R. Arkle for the Solar Pathfinder, K. A. Miller for algal identification, and the Cal Poly Biology Department for supplies and advice. Funding sources include Cal Poly College-Based Fees to S. Gravem, Office of Naval Research award # N00014-04-1-0436 to N. Adams, and the National Science Foundation Grant IBN—0417003 awarded to N. Adams. All experiments and collections complied with the current laws of the United States. The authors declare that they have no conflict of interest.

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  1. Sarah A. Gravem

    Present address: Bodega Marine Laboratory, University of California Davis, P.O. Box 247, Bodega Bay, CA, 94923, USA

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  1. Biological Sciences Department, California Polytechnic State University, San Luis Obispo, CA, 93407, USA

    Sarah A. Gravem & Nikki L. Adams

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Gravem, S.A., Adams, N.L. Sex and microhabitat influence the uptake and allocation of mycosporine-like amino acids to tissues in the purple sea urchin, Strongylocentrotus purpuratus . Mar Biol 159, 2839–2852 (2012). https://doi.org/10.1007/s00227-012-2045-z

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