618
Views
0
CrossRef citations to date
0
Altmetric
Original article

Potential energetic and oxygenic benefits to unstable photosymbiosis in the cladobranch slug, Berghia stephanieae (Nudibranchia, Aeolidiidae)

ORCID Icon, ORCID Icon, ORCID Icon & ORCID Icon
Pages 45-58 | Received 20 Apr 2023, Accepted 25 Jan 2024, Published online: 01 Mar 2024

References

  • Arboleda E, Hartenstein V, Martinez P, Reichert H, Sen S, Sprecher S, Bailly X. 2018. An emerging system to study photosymbiosis, brain regeneration, chronobiology, and behavior: the marine acoel Symsagittifera roscoffensis. BioEssays. 40(10). doi:10.1002/bies.201800107.
  • Armstrong EJ, Tanner RL, Stillman JH. 2019. High heat tolerance is negatively correlated with heat tolerance plasticity in nudibranch mollusks. Physiological and Biochemical Zoology. 92(4):430–444. doi:10.1086/704519.
  • Baker AC, Correa AMS, Cunning R. 2017. Diversity, distribution and stability of symbiodinium in reef corals of the eastern tropical pacific. In: Glynn PW, Manzello DP, Enochs IC, editors. Coral reefs of the eastern tropical pacific. Vol. 8. Dordrecht, Netherlands: Springer; p. 405–420. doi:10.1007/978-94-017-7499-4_13.
  • Bates D, Mächler M, Bolker B, Walker S. 2015. Fitting linear mixed-effects models using lme4. Journal of Statistical Software. 67(1):1–48. doi:10.18637/jss.v067.i01.
  • Bhagooli R, Hidaka M. 2004. Photoinhibition, bleaching susceptibility and mortality in two scleractinian corals, Platygyra ryukyuensis and Stylophora pistillata, in response to thermal and light stresses. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology. 137(3):547–555. doi:10.1016/j.cbpb.2003.11.008.
  • Biermann CH, Schinner GO, Strathmann RR. 1992. Influence of solar radiation, microalgal fouling, and current on deposition site and survival of embryos of a dorid nudibranch gastropod. Marine Ecology Progress Series. 86(3):205–215. http://www.jstor.org/stable/24830479.
  • Burghardt I, Evertsen J, Johnsen G, Wägele H. 2005. Solar powered seaslugs-mutualistic symbiosis of aeolid nudibranchia (Mollusca, Gastropoda, Opisthobranchia) with Symbiodinium. Symbiosis. 38(3):227–250. https://dalspace.library.dal.ca/bitstream/handle/10222/78144/VOLUME%2038-NUMBER%203-2005-PAGE%20227.pdf?sequence=1
  • Burghardt I, Wägele H. 2004. A new solar powered species of the genus Phyllodesmium Ehrenberg, 1831 (Mollusca: Nudibranchia: Aeolidoidea) from Indonesia with analysis of its photosynthetic activity and notes on biology. Zootaxa. 596(1):1–18. doi:10.11646/zootaxa.596.1.1.
  • Burghardt I, Wägele H. 2014. The symbiosis between the ‘solar-powered’ nudibranch Melibeengeli Risbec, 1937 (Dendronotoidea) and Symbiodinium sp. (Dinophyceae). Journal of Molluscan Studies. 80(5):508–517. doi:10.1093/mollus/eyu043.
  • Burgués Palau L, Senna G, Laetz EMJ. 2024. Crawl away from the light! Assessing behavioral and physiological photoprotective mechanisms in tropical solar-powered sea slugs exposed to natural light intensities. Marine Biology. 171:50. doi:10.1007/s00227-023-04350-w.
  • Carroll DJ, Kempf SC. 1990. Laboratory culture of the Aeolid Nudibranch Berghia verrucicornis (Mollusca, Opisthobranchia): some aspects of its development and life history. The Biological Bulletin. 179(3):243–253. doi:10.2307/1542315.
  • Cereja R. 2020. Critical thermal maxima in aquatic ectotherms. Ecological Indicators. 119:106856. doi:10.1016/j.ecolind.2020.106856.
  • Christa G, Pütz L, Sickinger C, Melo Clavijo J, Laetz EM, Greve C, Serôdio J. 2018. Photoprotective non-photochemical quenching does not prevent kleptoplasts from net photoinactivation. Frontiers in Ecology and Evolution. 6:121. doi:10.3389/fevo.2018.00121.
  • Clark KB. 1975. Nudibranch life cycles in the Northwest Atlantic and their relationship to the ecology of fouling communities. Helgoländer Wissenschaftliche Meeresuntersuchungen. 27(1):28–69. doi:10.1007/BF01611686.
  • Cowles RB, Bogert CM. 1944. A preliminary study of the thermal requirements of desert reptiles. Bulletin of the AMNH. 83(5):261–296.
  • Cruz S, Calado R, Serôdio J, Cartaxana P. 2013. Crawling leaves: photosynthesis in sacoglossan sea slugs. Journal of Experimental Botany. 64(13):3999–4009. doi:10.1093/jxb/ert197.
  • Davy SK, Allemand D, Weis VM. 2012. Cell biology of cnidarian-dinoflagellate symbiosis. Microbiology and Molecular Biology Reviews. 76(2):229–261. doi:10.1128/MMBR.05014-11.
  • Di Marzo V, Marin A, Vardaro RR, De Petrocellis L, Villani G, Cimino G. 1993. Histological and biochemical bases of defense mechanisms in four species of Polybranchioidea ascoglossan molluscs. Marine Biology. 117(3):367–380. doi:10.1007/BF00349312.
  • Dinno A. 2017. dunn.test: Dunn's test of multiple comparisons using rank sums. R package version 1.3.5. https://CRAN.R-project.org/package=dunn.test.
  • Douglas AE, Smith DC. 2019. Intracellular space as oligogenetic ecosystem. In: Schenk HEA, Schwemmler W, editors. Proceedings: Second International Colloquium on Endocytobiology; April 10–15, 1983; Tübingen, Germany, 2. De Gruyter. p. 631–648. doi:10.1515/9783110841237-067.
  • Durán-Fuentes J, Gracia A, González-Muñoz R. 2022. Sea anemones (cnidaria, anthozoa, actiniaria) in high sedimentation environments influenced by the Magdalena river (Colombian Caribbean). Anais da Academia Brasileira de Ciências. 94. doi:10.1590/0001-3765202120190862.
  • Edmunds PJ, Tsounis G, Boulon R, Bramanti L. 2018. Long-term variation in light intensity on a coral reef. Coral Reefs. 37:955–965. doi:10.1007/s00338-018-1721-y.
  • Fitt W, Brown B, Warner M, Dunne R. 2001. Coral bleaching: Interpretation of thermal tolerance limits and thermal thresholds in tropical corals. Coral Reefs. 20(1):51–65. doi:10.1007/s003380100146.
  • Furfaro G, Mariottini P. 2020. A new Dondice Marcus Er. 1958 (Gastropoda: Nudibranchia) from the Mediterranean Sea reveals interesting insights into the phylogenetic history of a group of Facelinidae taxa . Zootaxa. 4731(1):001–022. doi:10.11646/zootaxa.4731.1.1.
  • Garrett TA, Schmeitzel JL, Klein JA, Hwang JJ, Schwarz JA. 2013. Comparative lipid profiling of the cnidarian aiptasia pallida and its dinoflagellate symbiont. PLoS One. 8(3):e57975. doi:10.1371/journal.pone.0057975.
  • Grajales A, Rodríguez E. 2014. Morphological revision of the genus Aiptasia and the family Aiptasiidae (Cnidaria, Actiniaria, Metridioidea). Zootaxa. 3826(1):55–100. doi:10.11646/zootaxa.3826.1.2.
  • Grajales A, Rodríguez E. 2019. Case 3790 – proposed review of opinion 2404 and reconsideration of Case 3633: Dysactis pallida Agassiz in Verrill, 1864 (currently Exaiptasia pallida; Cnidaria, Anthozoa, Hexacorallia, Actiniaria): Proposed precedence over Exaiptasia diaphana (Rapp, 1829). The Bulletin of Zoological Nomenclature. 76(1):127–131. doi:10.21805/bzn.v76.a036.
  • Havenhand JN, Todd CD. 1988. Physiological ecology of Adalariaproxima (Alder et Hancock) and Onchidoris muricata (Mtiller) (Gastropoda: Nudibranchia). I. Feeding, growth, and respiration. Journal of Experimental Marine Biology and Ecology. 118:151–172. doi:10.1016/0022-0981(88)90237-7.
  • Hoegh-Guldberg O, Jones R. 1999. Photoinhibition and photoprotection in symbiotic dinoflagellates from reef-building corals. Marine Ecology Progress Series. 183:73–86. doi:10.3354/meps183073.
  • Jeong HJ, Yoo YD, Kang NS, Lim AS, Seong KA, Lee SY, Lee MJ, Lee KH, Kim HS, Shin W, et al. 2012. Heterotrophic feeding as a newly identified survival strategy of the dinoflagellate symbiodinium. Proceedings of the National Academy of Sciences. 109(31):12604–12609. doi:10.1073/pnas.1204302109.
  • Kempf SC. 1984. Symbiosis between the zooxanthella symbiodinium (=gymnodinium) microadriaticum (freudenthal) and four species of nudibranchs. The Biological Bulletin. 166(1):110–126. doi:10.2307/1541435.
  • Kristof A, Klussmann-Kolb A. 2010. Neuromuscular development of aeolidiella stephanieae valdez, 2005 (mollusca, gastropoda, nudibranchia). Frontiers in Zoology. 7:5. doi:10.1186/1742-9994-7-5.
  • Laetz EM, Moris VC, Moritz L, Haubrich AN, Wägele H. 2017. Photosynthate accumulation in solar-powered sea slugs – starving slugs survive due to accumulated starch reserves. Frontiers in Zoology. 14(4):1–9. doi:10.1186/s12983-016-0186-5.
  • Laetz EMJ, Wägele H. 2019. Comparing amylose production in two solar-powered sea slugs: the sister taxa Elysia timida and E. cornigera (Heterobranchia: Sacoglossa). Journal of Molluscan Studies. 85(1):166–171. doi:10.1093/mollus/eyy047.
  • Ledford HK, Niyogi KK. 2005. Singlet oxygen and photo-oxidative stress management in plants and algae. Plant, Cell & Environment. 28(8):1037–1045. doi:10.1111/j.1365-3040.2005.01374.x.
  • Lenth RV. 2021. emmeans: estimated marginal means, aka least-squares means. R package version 1.6.0. https://CRAN.R-project.org/package=emmeans.
  • Lesser MP. 2006. Oxidative stress in marine environments: biochemistry and physiological ecology. Annual Review of Physiology. 68(1):253–278. doi:10.1146/annurev.physiol.68.040104.110001.
  • Lutterschmidt WI, Hutchison VH. 1997. The critical thermal maximum: history and critique. Canadian Journal of Zoology. 75(10):1561–1574. doi:10.1139/z97-783.
  • Mantelatto MC, Oliveira AESD, Menegola C, Casares FA, Creed JC. 2020. Depth and grazing intensity are the main drivers of subtidal hardground benthic community structure on tropical south Atlantic reefs. Marine Ecology. 41(3):1–13. doi:10.1111/maec.12586.
  • Marín A, Ros J. 1991. Presence of intracellular zooxanthellae in Mediterranean nudibranchs. Journal of Molluscan Studies. 57(4):87–101. doi:10.1093/mollus/57.Supplement_Part_4.87.
  • Marshall DJ, Dong Y, McQuaid CD, Williams GA. 2011. Thermal adaptation in the intertidal snail Echinolittorina malaccana contradicts current theory by revealing the crucial roles of resting metabolism. Journal of Experimental Biology. 214(21):3649–3657. doi:10.1242/jeb.059899.
  • Marshall DJ, McQuaid CD. 2011. Warming reduces metabolic rate in marine snails: adaptation to fluctuating high temperatures challenges the metabolic theory of ecology. Proceedings of the Royal Society B: Biological Sciences. 278(1703):281–288. doi:10.1098/rspb.2010.1414.
  • Melo Clavijo J, Donath A, Serôdio J, Christa G. 2018. Polymorphic adaptations in metazoans to establish and maintain photosymbioses. Biological Reviews. 93(4):2006–2020. doi:10.1111/brv.12430.
  • Melo Clavijo J, Sickinger C, Bleidißel S, Gasparoni G, Tierling S, Preisfeld A, Christa G. 2022. The nudibranch Berghia stephanieae (Valdés, 2005) is not able to initiate a functional symbiosome-like environment to maintain Breviolum minutum (JE Parkinson & LaJeunesse 2018). Frontiers in Marine Science. 9. doi:10.22028/D291-38136.
  • Mies M, Voolstra CR, Castro CB, Pires DO, Calderon EN, Sumida PY. 2017. Expression of a symbiosis-specific gene in Symbiodinium type A1 associated with coral, nudibranch and giant clam larvae. Royal Society Open Science. 4(5):170253. doi:10.1098/rsos.170253.
  • Monteiro EA, Güth AZ, Banha TNS, Sumida PYG, Mies M. 2019. Evidence against mutualism in an aeolid nudibranch associated with symbiodiniaceae dinoflagellates. Symbiosis. 79(2):183–189. doi:10.1007/s13199-019-00632-4.
  • Nybakken J, McDonald G. 1981. Feed mechanisms of West American nudibranchs feeding on Byrozoa, Cnidaria and Ascidiacea, with special respect to the radula. Malacologia. 20(2):439–449.
  • Parker GM. 1984. Dispersal of zooxanthellae on coral reefs by predators on cnidarians. The Biological Bulletin. 167(1):159–167. doi:10.2307/1541344.
  • Pörtner HO. 2002. Climate variations and the physiological basis of temperature dependent biogeography: systemic to molecular hierarchy of thermal tolerance in animals. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology. 132(4):739–761. doi:10.1016/S1095-6433(02)00045-4.
  • Pospíšil P. 2016. Production of reactive oxygen species by photosystem II as a response to light and temperature stress. Frontiers in Plant Science. 7. doi:10.3389/fpls.2016.01950.
  • Potts GW. 1983. The respiration of Onchidorisbilamellata and Archidorispseudoargus (Doridacea). Journal of the Marine Biological Association of the United Kingdom. 63(2):399–407. doi:10.1017/S0025315400070752.
  • Przeslawski R, Davis A, Benkendorff K. 2004. Effects of ultraviolet radiation and visible light on the development of encapsulated molluscan embryos. Marine Ecology Progress Series. 268:151–160. doi:10.3354/meps268151.
  • Quinlan PD, Katz PS. 2022. State-dependent, visually-guided behaviors in the nudibranch Berghia stephanieae. bioRxiv. doi:10.1101/2022.10.24.513581.
  • Rädecker N, Pogoreutz C, Gegner HM, Cárdenas A, Roth F, Bougoure J, Guagliardo P, Wild C, Pernice M, Raina J-B, et al. 2021. Heat stress destabilizes symbiotic nutrient cycling in corals. Proceedings of the National Academy of Sciences. 118(5):e2022653118. doi:10.1073/pnas.2022653118.
  • Ralph P, Gademann R, Larkum A, Schreiber U. 1999. In situ underwater measurements of photosynthetic activity of coral zooxanthellae and other reef-dwelling dinoflagellate endosymbionts. Marine Ecology Progress Series. 180:139–147. doi:10.3354/meps180139.
  • R Core Team. 2022. R: a language and environment for statistical computing. Vienna: R Foundation for Statistical Computing. https://www.R-project.org/.
  • Rola M, Frankenbach S, Bleidissel S, Sickinger C, Donath A, Frommlet JC, Greve C, Serôdio J, Preisfeld A, Melo Clavijo J, Christa G. 2022. Cladobranchia (gastropoda, nudibranchia) as a promising model to understand the molecular evolution of photosymbiosis in animals. Frontiers in Marine Science. 8. doi:10.3389/fmars.2021.745644.
  • R Studio Team. 2020. Rstudio: integrated development environment for R. Boston (MA): RStudio, Inc. http://www.rstudio.com.
  • Rumpho ME, Pelletreau KN, Moustafa A, Bhattacharya D. 2011. The making of a photosynthetic animal. Journal of Experimental Biology. 214(2):303–311. doi:10.1242/jeb.046540.
  • Smith DA, Sebens P. 1983. The physiological ecology of growth and reproduction in Onchidoris aspera (Alder & Hancock) (Gastropoda: Nudibranchia). Journal of Experimental Marine Biology and Ecology. 72:287–304. doi:10.1016/0022-0981(83)90112-0.
  • Sokolova IM, Pörtner HO. 2001. Physiological adaptations to high intertidal life involve improved water conservation abilities and metabolic rate depression in Littorina saxatilis. Marine Ecology Progress Series. 224:171–186. doi:10.3354/meps224171.
  • Sokolova IM, Pörtner H-O. 2003. Metabolic plasticity and critical temperatures for aerobic scope in a eurythermal marine invertebrate (Littorina saxatilis, Gastropoda: Littorinidae) from different latitudes. Journal of Experimental Biology. 206(1):195–207. doi:10.1242/jeb.00054.
  • Stanley GD. 2006. Ecology: photosymbiosis and the evolution of modern coral reefs. Science. 312(5775):857–858. doi:10.1126/science.1123701.
  • Steen RG. 1986. Evidence for heterotrophy by zooxanthellae in symbiosis with Aiptasia pulchella. The Biological Bulletin. 170(2):267–278. doi:10.2307/1541808.
  • Stenseng E, Braby CE, Somero GN. 2005. Evolutionary and acclimation-induced variation in the thermal limits of heart function in congeneric Marine Snails (Genus Tegula): implications for vertical zonation. The Biological Bulletin. 208(2):138–144. doi:10.2307/3593122.
  • Storch D, Menzel L, Frickenhaus S, Pörtner H-O. 2014. Climate sensitivity across marine domains of life: limits to evolutionary adaptation shape species interactions. Global Change Biology. 20(10):3059–3067. doi:10.1111/gcb.12645.
  • Sunagawa S, Wilson EC, Thaler M, Smith ML, Caruso C, Pringle JR, Weis VM, Medina M, Schwarz JA. 2009. Generation and analysis of transcriptomic resources for a model system on the rise: the sea anemone Aiptasia pallida and its dinoflagellate endosymbiont. BMC Genomics. 10(1):258. doi:10.1186/1471-2164-10-258.
  • USGS. 2011. Dissolved oxygen solubility tables. Washington, DC, USA: US Department of the Interior. [accessed throughout 202] https://water.usgs.gov/water-resources/software/DOTABLES/
  • Verberk WCEP, Overgaard J, Ern R, Bayley M, Wang T, Boardman L, Terblanche JS. 2016. Does oxygen limit thermal tolerance in arthropods? A critical review of current evidence. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology. 192:64–78. doi:10.1016/j.cbpa.2015.10.020.
  • Wägele H. 2004. Potential key characters in Opisthobranchia (Gastropoda, Mollusca) enhancing adaptive radiation. Organisms Diversity & Evolution. 4(3):175–188. doi:10.1016/j.ode.2004.03.002.
  • Watson WH, Bourque KMF, Sullivan JR, Miller M, Buell A, Kallins MG, Curtis NE, Pierce SK, Blackman E, Urato S, Newcomb JM. 2021. The digestive diverticula in the carnivorous nudibranch, melibe leonina, do not contain photosynthetic symbionts. Integrative Organismal Biology. 3(1):1–11. doi:10.1093/iob/obab015.
  • Weis VM, Davy SK, Hoegh-Guldberg O, Rodriguez-Lanetty M, Pringle JR. 2008. Cell biology in model systems as the key to understanding corals. Trends in Ecology & Evolution. 23(7):369–376. doi:10.1016/j.tree.2008.03.004.
  • Wickham H. 2016. Ggplot2: elegant graphics for data analysis. New York: Springer-Verlag. ISBN 978-3-319-24277-4, https://ggplot2.tidyverse.org.
  • Woods HA, Moran AL, Atkinson D, Audzijonyte A, Berenbrink M, Borges FO, Burnett KG, Burnett LE, Coates CJ, Collin R, et al. 2022. Integrative approaches to understanding organismal responses to aquatic deoxygenation. The Biological Bulletin. 243(2):85–103. doi:10.1086/722899.
  • WoRMS Editorial Board. 2023. World register of Marine species. https://www.marinespecies.org at VLIZ. [accessed 2023 December 19].