Foxed intra- and interspecific differentiation in Leptogorgia (Octocorallia: Gorgoniidae). A description of a new species based on multiple sources of evidence

Authors

DOI:

https://doi.org/10.3989/scimar.04509.01C

Keywords:

incomplete lineage sorting, hybridization, ITS, mtMutS, 28S, CoxII-Igr-CoxI, Igr, Ecuador

Abstract


The challenges of delimiting and identifying marine invertebrate species impede estimations of true biodiversity. This is particularly true in the case of gorgonian diversity, in which only classical morphological characters (e.g. branching pattern, size and colouration of the colony and sclerites, etc.), which can be homoplastic and continuous, have been used. In this study, using an integrative taxonomic approach, we analysed two morphs initially considered as two eco-typical variants of Leptogorgia alba Duchassaing and Michelotti, 1864, living sympatrically in the littoral area of Ecuador. We explored the use of classical morphological and morphometric characters to delimit species in combination with the analyses of molecular markers (mtMutS, CoxII-Igr-CoxI, ITSs, and 28S rRNA) to infer phylogenetic relationships. Based on our results, two species should be considered, L. alba and a new species, L. manabiensis n. sp., which showed distinguishing morphological features that cannot be attributed to phenotypic plasticity. Both species also showed significant differences in morphometric, non-correlated characters in all size classes. The phylogenetic analyses showed a polyphyletic L. alba - L. manabiensis n. sp. species complex, and ancestral polymorphism and incomplete lineage sorting as possible evolutionary processes leading to this pattern. In conclusion, the combination of morphological and morphometric evidences provides the best support for the identification and delimitation of these challenging species. In addition, molecular analyses, mainly supported by nuclear markers, allow fundamental aspects of the evolutionary history of these organisms to be discerned.

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References

Abràmoff M.D., Magalhães P.J., Ram S.J. 2004. Image processing with imageJ. Biophotonics. Int. 11: 36-41.

Aguilar C., Sánchez J.A. 2007. Molecular morphometrics: Contribution of ITS2 sequences and predicted RNA secondary structures to octocoral systematics. Bull. Mar. Sci. 81: 335-349.

Alderslade P. 1998. Revisionary systematics in the gorgonian family Isididae: with descriptions of numerous new taxa (Coelenterata: Octocorallia). Rec. West. Aust. Museum. 55: 1-359.

Alfaya J.E.F., Bigatti G., Kajihara H., et al. 2015. DNA barcoding supports identification of Malacobdella species (Nemertea: Hoplonemertea). Zool. Stud. 54: 10. https://doi.org/10.1186/s40555-014-0086-3

Ament-Velásquez S.L., Breedy O., Cortés J., et al. 2016. Homoplasious colony morphology and mito-nuclear phylogenetic discordance among Eastern Pacific octocorals. Molec. Phylogenet. Evol. 98: 373-381. https://doi.org/10.1016/j.ympev.2016.02.023 PMid:26953740

Anderson M.J. 2001. A new method for non-parametric multivariate analysis of variance. Austral. Ecol. 26: 32-46.

Anderson M.J. 2006. Distance-based tests for homogeneity of multivariate dispersions. Biometrics 62: 245-253. https://doi.org/10.1111/j.1541-0420.2005.00440.x PMid:16542252

Anderson M.J., Gorley R.N., Clarke K.R. 2008. PERMANOVA+ for PRIMER: Guide to Software and Statistical Methods. PRIMER-E, Plymouth, UK.

Bayer F.M. 1961. The shallow-water Octocorallia of the West Indian region. A manual for marine biologists. Stud. Fauna. Curacao. Caribb. Islands. 12: 1-373.

Bayer F.M. 2000. A new species of Leptogorgia from the eastern Pacific (Coelenterata: Octocorallia: Holaxonia). Proc. Biol. Soc. Washingt. 113: 609-616.

Bayer F.M., Stefani J. 1989. Primnoidae de Nouvelle-Calédonie. Bull. Mus. Nat. His. Nat. Paris. 4 ser., Sect A. 3: 449-476.

Bayer F.M., Grasshoff M., Verseveldt J. 1983. Illustrated trilingual glossary of morphological terms applied to Octocorallia. Brill E.J. (ed), Leiden.

Bielschowsky E. 1929. Die Gorgonarien Westindien. 6. Die Familie Gorgoniidae, zugleich eine Revision. Zool. Jahrbücher. Suppl. 16: 63-234.

Brazeau D.A., Lasker H.R. 1988. Inter- and intraspecific variation in gorgonian colony morphology: quantifying branching patterns in arborescent animals. Coral Reefs 7: 139-143. https://doi.org/10.1007/BF00300973

Breedy O., Guzman H.M. 2003. Octocorals from Costa Rica: The genus Pacifigorgia (Coelenterata: Octocorallia: Gorgoniidae). Zootaxa 281: 1-60. https://doi.org/10.11646/zootaxa.281.1.1

Breedy O., Guzman H.M. 2005. A new species of Leptogorgia (Coelenterata: Octocorallia: Gorgoniidae) from the shallow waters of the eastern Pacific. Zootaxa 899: 1-11. https://doi.org/10.11646/zootaxa.899.1.1

Breedy O., Guzman H.M. 2007. A revision of the genus Leptogorgia Milne-Edwards and Haime, 1857 (Coelenterata: Octocorallia: Gorgoniidae) in the Eastern Pacific. Zootaxa 1419: 1-90. https://doi.org/10.11646/zootaxa.1419.1.1

Breedy O., Abeytia R., Guzman H.M. 2012. A new species of Leptogorgia (Cnidaria: Anthozoa: Octocorallia) from the Mexican Pacific coast. Bull. Mar. Sci. 88: 319-325. https://doi.org/10.5343/bms.2011.1103

Calvo M., Templado J., Oliverio M., et al. 2009. Hidden Mediterranean biodiversity: Molecular evidence for a cryptic species complex within the reef building vermetid gastropod Dendropoma petraeum (Mollusca: Caenogastropoda). Biol. J. Linn. Soc. 96: 898-912. https://doi.org/10.1111/j.1095-8312.2008.01167.x

Carlon D.B., Budd F.A. 2002. Incipient speciation across a depth gradient in a scleractinian coral? Evolution 56: 2227-2242. https://doi.org/10.1111/j.0014-3820.2002.tb00147.x PMid:12487353

Carstens B.C., Knowles L.L. 2007. Estimating species phylogeny from gene-tree probabilities despite incomplete lineage sorting: an example from Melanoplus grasshoppers. Syst. Biol. 56: 400-411. https://doi.org/10.1080/10635150701405560 PMid:17520504

Clarke K.R., Gorley R.N. 2006. PRIMER v6: User manual/tutorial. PRIMER-E. 192 pp.

Costantini F., Gori A., Lopez-González P., et al. 2016. Limited genetic connectivity between gorgonian morphotypes along a depth gradient. PLoS One 11: e0160678. https://doi.org/10.1371/journal.pone.0160678 PMid:27490900 PMCid:PMC4973999

Dayrat B. 2005. Towards integrative taxonomy. Biol. J. Linn. Soc. 85: 407-415. https://doi.org/10.1111/j.1095-8312.2005.00503.x

Devictor S.T., Morton S.L. 2010. Identification guide to the shallow water (0-200 m) octocorals of the South Atlantic Bight. Zootaxa 62: 1-62.

Diekmann O.E., Bak R.P.M., Stam W.T., et al. 2001. Molecular genetic evidence for probable reticulate speciation in the coral genus Madracis from a Caribbean fringing reef slope. Mar. Biol. 139: 221-233. https://doi.org/10.1007/s002270100584

Dinc? V., Lukhtanov V.A., Talavera G., et al. 2011. Unexpected layers of cryptic diversity in wood white Leptidea butterflies. Nat. Commun. 2: 324.

Duchassaing P., Michelotti J. 1864. Supplément au Mémoire sur les coralliaires des Antilles. Extr. Mém. Acad. Sci. Turin 2: 1-112.

Eberle J., Warnock R.C.M., Ahrens D. 2016. Bayesian species delimitation in Pleophylla chafers (Coleoptera) - the importance of prior choice and morphology. BMC. Evol. Biol. 16: 94. https://doi.org/10.1186/s12862-016-0659-3 PMid:27149864 PMCid:PMC4858874

Flot J.F., Licuanan W.Y., Nakano Y., et al. 2008. Mitochondrial sequences of Seriatopora corals show little agreement with morphology and reveal the duplication of a tRNA gene near the control region. Coral Reefs 27: 789-794. https://doi.org/10.1007/s00338-008-0407-2

Forsman Z., Conception G., Haverkort R. 2010. Is Montipora dilatata an endangered coral species or an ecotype? Genes and skeletal microstructure lump seven Hawaiian species into four groups. NOAA Rep: 20.

France S.C., Hoover L.L. 2002. DNA sequences of the mitochondrial COI gene have low levels of divergence among deep-sea octocorals (Cnidaria: Anthozoa). Hydrobiologia 471: 149-155. https://doi.org/10.1023/A:1016517724749

Gori A., Bramanti L., López-González P.J., et al. 2012. Characterization of the zooxanthellate and azooxanthellate morphotypes of the Mediterranean gorgonian Eunicella singularis. Mar. Biol. 159: 1485-1496. https://doi.org/10.1007/s00227-012-1928-3

Grasshoff M. 1988. The genus Leptogorgia (Octocorallia: Gorgoniidae) in West Africa. Atl. Rep. 14: 91-147.

Guindon S., Gascuel O. 2003. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst. Biol. 52: 696-704. https://doi.org/10.1080/10635150390235520 PMid:14530136

Guzman H.M., Breedy O. 2008. Leptogorgia christiae (Octocorallia: Gorgoniidae) a new shallow gorgonian from Pacific Panama. Mar. Biol. Assoc. U.K. 88: 719-722. https://doi.org/10.1017/S0025315408001240

Hatta M., Fukami H., Wang W., et al. 1999. Reproductive and genetic evidence for a reticulate evolutionary history of mass-spawning corals. Mol. Biol. Evol. 16: 1607-1613. https://doi.org/10.1093/oxfordjournals.molbev.a026073 PMid:10555292

Hellberg M.E. 2006. No variation and low synonymous substitution rates in coral mtDNA despite high nuclear variation. BMC Evol. Biol. 6: 24. https://doi.org/10.1186/1471-2148-6-24 PMid:16542456 PMCid:PMC1431588

Henning F., Meyer A. 2014. The evolutionary genomics of cichlid fishes: explosive speciation and adaptation in the postgenomic era. Annu. Rev. Genomics. Hum. Genet. 15: 417-441. https://doi.org/10.1146/annurev-genom-090413-025412 PMid:24898042

Hoelzer G., Melnick D.J. 1994. Patterns of speciation and limits to phylogenetic resolution. Trends. Ecol. Evol. 9: 104-107. https://doi.org/10.1016/0169-5347(94)90207-0

Horton R.E. 1945. Erosional development of streams and their drainage basins; Hydrophysical approach to quantitative morphology. Bull. Geol. Soc. Am. 56: 275-370. https://doi.org/10.1130/0016-7606(1945)56[275:EDOSAT]2.0.CO;2

Horvath E.A. 2011. An unusual new "sea fan" from the northeastern Pacific Ocean (Cnidaria: Octocorallia: Gorgoniidae). Proc. Biol. Soc. Washingt. 124: 45-52. https://doi.org/10.2988/10-27.1

Huelsenbeck J.P., Ronquist F. 2001. MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17: 754-755. https://doi.org/10.1093/bioinformatics/17.8.754 PMid:11524383

Hugall A, Stanton J, Moritz C. 1999. Reticulate evolution and the origins of ribosomal internal transcribed spacer diversity in apomictic Meloidogyne. Mol. Biol. Evol. 16: 157-164. https://doi.org/10.1093/oxfordjournals.molbev.a026098 PMid:10028283

Lewis J.C., Wallis E.V. 1991. The function of surface sclerites in gorgonians (Coelenterata, Octocorallia). Biol. Bull. 181: 275-288. https://doi.org/10.2307/1542099

López-González P.J., Grinyó J., Gili J.M. 2015. Chironephthya mediterranea n. sp. (Octocorallia, Alcyonacea, Nidaliidae), the first species of the genus discovered in the Mediterranean Sea. Mar. Biodiv. 45: 667-688. https://doi.org/10.1007/s12526-014-0269-5

Lumley L.M., Sperling F.A.H. 2010. Integrating morphology and mitochondrial DNA for species delimitation within the spruce budworm (Choristoneura fumiferana) cryptic species complex (Lepidoptera: Tortricidae). Syst. Entomol. 35: 416-428. https://doi.org/10.1111/j.1365-3113.2009.00514.x

McArdle B.H., Anderson M.J. 2001. Fitting multivariate models to community data: A comment on distance-based redundancy analysis. Ecol. Soc. Am. 82: 290-297. https://doi.org/10.1890/0012-9658(2001)082[0290:FMMTCD]2.0.CO;2

McFadden C.S., Hutchinson M.B. 2004. Molecular evidence for the hybrid origin of species in the soft coral genus Alcyonium (Cnidaria: Anthozoa: Octocorallia). Mol. Ecol. 13: 1495-1505. https://doi.org/10.1111/j.1365-294X.2004.02167.x PMid:15140093

McFadden C.S., van Ofwegen L.P. 2013. A second, cryptic species of the soft coral genus Incrustatus (Anthozoa: Octocorallia: Clavulariidae) from Tierra del Fuego, Argentina, revealed by DNA barcoding. Helgol. Mar. Res. 67: 137-147. https://doi.org/10.1007/s10152-012-0310-7

McFadden C.S., Tullis I.D., Hutchinson M.B., et al. 2004. Variation in coding (NADH dehydrogenase subunits 2, 3, and 6) and noncoding intergenic spacer regions of the mitochondrial genome in Octocorallia (Cnidaria: Anthozoa). Mar. Biotechnol. 6: 516-526. https://doi.org/10.1007/s10126-002-0102-1 PMid:15723254

McFadden C.S., France S.C., Sánchez J.A., et al. 2006. A molecular phylogenetic analysis of the Octocorallia (Cnidaria: Anthozoa) based on mitochondrial protein-coding sequences. Mol. Phylogenet. Evol. 41: 513-527. https://doi.org/10.1016/j.ympev.2006.06.010 PMid:16876445

McFadden C.S., Sánchez J.A., France S.C. 2010. Molecular phylogenetic insights into the evolution of octocorallia: A review. Integr. Comp. Biol. 50: 389-410. https://doi.org/10.1093/icb/icq056 PMid:21558211

McFadden C.S., Benayahu Y., Pante E., et al. 2011. Limitations of mitochondrial gene barcoding in Octocorallia. Mol. Ecol. Resour. 11: 19-31. https://doi.org/10.1111/j.1755-0998.2010.02875.x PMid:21429097

Meyer C.P., Paulay G. 2005. DNA barcoding: Error rates based on comprehensive sampling. PLoS Biol. 3: 1-10. https://doi.org/10.1371/journal.pbio.0030422 PMid:16336051 PMCid:PMC1287506

Milne-Edwards H., Haime J. 1857. Histoire naturelle des coralliaires: ou, Polypes proprement dits. à la Libraire Encyclopédique de Roret, Paris.

Mutanen M., Pretorius E. 2007. Subjective visual evaluation vs. traditional and geometric morphometrics in species delimitation: A comparison of moth genitalia. Syst. Entomol. 32: 371-386. https://doi.org/10.1111/j.1365-3113.2006.00372.x

Nater A., Burri R., Kawakami T., et al. 2015. Resolving evolutionary relationships in closely related species with whole-genome sequencing data. Syst. Biol. 46: 1-54. https://doi.org/10.1093/sysbio/syv045

Padial J.M., Miralles A., de la Riva I., et al. 2010. The integrative future of taxonomy. Front. Zool. 7: 16. https://doi.org/10.1186/1742-9994-7-16 PMid:20500846 PMCid:PMC2890416

Pérez C.D., Neves B.M., Cordeiro R.T., et al. 2016. Diversity and Distribution of Octocorallia. In: Goffredo S., Dubinsky Z. (eds) The Cnidaria, Past, Present and Future. Springer International Publishing, Cham, pp 109-123. https://doi.org/10.1007/978-3-319-31305-4_8 PMid:26626079 PMCid:PMC4936798

Posada D. 2008. jModelTest: Phylogenetic model averaging. Mol. Biol. Evol. 25: 1253-1256. https://doi.org/10.1093/molbev/msn083 PMid:18397919

Rambaut A., Drummond A. 2007. Tracer v1.4. http://beast.bio.ed.ac.uk/Tracer

Rocha-Olivares A., Fleeger J.W., Foltz D.W. 2001. Decoupling of molecular and morphological evolution in deep lineages of a Meiobenthic harpacticoid copepod. Mol. Biol. Evol. 18: 1088-1102. https://doi.org/10.1093/oxfordjournals.molbev.a003880 PMid:11371597

Rossi S., Gili J.M., Garrofé X. 2011. Net negative growth detected in a population of Leptogorgia sarmentosa: quantifying the biomass loss in a benthic soft bottom-gravel gorgonian. Mar. Biol. 158: 1631-1643. https://doi.org/10.1007/s00227-011-1675-x

Sánchez J.A. 2009. Systematics of the candelabrum gorgonian corals (Eunicea Lamouroux; Plexauridae; Octocorallia; Cnidaria). Zool. J. Linn. Soc. 157: 237-263. https://doi.org/10.1111/j.1096-3642.2008.00515.x

Sánchez J.A., Wirshing H.H. 2005. A field key to the identification of tropical western Atlantic zooxanthellate octocorals (Octocorallia: Cnidaria). Caribb. J. Sci. 41: 508-522.

Sánchez J.A., McFadden C.S., France S.C., et al. 2003. Molecular phylogenetic analyses of shallow-water Caribbean octocorals. Mar. Biol. 142: 975-987. https://doi.org/10.1007/s00227-003-1018-7

Sánchez J.A., Aguilar C., Dorado D., et al. 2007. Phenotypic plasticity and morphological integration in a marine modular invertebrate. BMC Evol. Biol. 7: 122. https://doi.org/10.1186/1471-2148-7-122 PMid:17650324 PMCid:PMC1959521

Schwarzfeld M.D., Sperling F.A.H. 2014. Species delimitation using morphology, morphometrics, and molecules: Definition of the Ophion scutellaris Thomson species group, with descriptions of six new species (Hymenoptera, Ichneumonidae). Zookeys 114: 59-114. https://doi.org/10.3897/zookeys.462.8229 PMid:25589855 PMCid:PMC4284433

Soler-Hurtado M.M., López-González P.J. 2012. Two new gorgonian species (Anthozoa: Octocorallia: Gorgoniidae) from Ecuador (Eastern Pacific). Mar. Biol. Res. 8: 380-387. https://doi.org/10.1080/17451000.2011.634814

Soler-Hurtado M.M., López-González P.J., Mu-oz J., et al. 2016. New records of the genera Leptogorgia, Pacifigorgia and Eugorgia (Octocorallia, Gorgoniidae) from Ecuador and description of a new species. Sci. Mar. 80: 369-394. https://doi.org/10.3989/scimar.04392.14A

Stefani F., Benzoni F., Pichon M., et al. 2008. A multidisciplinary approach to the definition of species boundaries in branching species of the coral genus Psammocora (Cnidaria, Scleractinia). Zool. Scr. 37: 71-91.

Strahler A.N. 1954. Quantitative geomorphology of erosional landscape. In: 19th Intern. Geol. Cong. Algiers, pp. 341-354.

Swofford D.L. 2003. PAUP*. Phylogenetic Analysis Using Parsimony (*and other methods), version 4. Sinauer Associates, Sunderland, Massachusetts. PMid:18428704

Valenciennes A. 1846. Zoophytes. In: Dupetit-Thouars A. (ed) Voyage autour du monde sur la frégate la Vénus, pendant les années 1836-1839. Atlas de Zoologie. Publié par ordre Du Roi, Paris, pp. 1-15.

van Oppen M.J., McDonald B.J., Willis B., et al. 2001. The evolutionary history of the coral genus Acropora (Scleractinia, Cnidaria) based on a mitochondrial and a nuclear marker: reticulation, incomplete lineage sorting, or morphological convergence? Mol. Biol. Evol. 18: 1315-1329. https://doi.org/10.1093/oxfordjournals.molbev.a003916 PMid:11420370

van Velzen R., Weitschek E., Felici G., et al. 2012. DNA barcoding of recently diverged species: Relative performance of matching methods. PLoS One 7: e30490. https://doi.org/10.1371/journal.pone.0030490 PMid:22272356 PMCid:PMC3260286

Vargas S., Breedy O., Guzman H.M. 2010. The phylogeny of Pacifigorgia (Coelenterata, Octocorallia, Gorgoniidae): a case study of the use of continuous characters in the systematics of the Octocorallia. Zoosystema 32: 5-18. https://doi.org/10.5252/z2010n1a1

Vargas S., Guzman H.M., Breedy O., et al. 2014. Molecular phylogeny and DNA barcoding of tropical eastern Pacific shallow-water gorgonian octocorals. Mar. Biol. 161: 1027-1038. https://doi.org/10.1007/s00227-014-2396-8

Vermeij M.J.A., Sandin S.A., Samhouri J.F. 2007. Local habitat distribution determines the relative frequency and interbreeding potential for two Caribbean coral morphospecies. Evol. Ecol. 21: 27-47. https://doi.org/10.1007/s10682-006-9122-z

Verrill A.E. 1868. Notes on Radiata in the Museum of Yale College, Number 6, Second. Transactions of the Connecticut Academy of Arts and Sciences.

Viladrich N., Gori A., Gili J.M. 2016. Fast growth rate in a young colony of the Mediterranean gorgonian Eunicella singularis. Mar. Biodiv. 158: 1631-1643. https://doi.org/10.1007/s12526-016-0554-6

Vollmer S.V., Palumbi S.R. 2004. Testing the utility of internally transcribed spacer sequences in coral phylogenetics. Mol. Ecol. 13: 2763-2772. https://doi.org/10.1111/j.1365-294X.2004.02265.x PMid:15315687

Weinbauer M.G., Branko V. 1995. Morphological variations in the Mediterranean sea fan Eunicella cavolini (Coelenterata: Gorgonacea) in relation to exposure, colony size and colony region. Bull. Mar. Sci. 56: 283-295.

Wiemers M., Fiedler K. 2007. Does the DNA barcoding gap exist? - a case study in blue butterflies (Lepidoptera: Lycaenidae). Front. Zool. 4: 8. https://doi.org/10.1186/1742-9994-4-8 PMid:17343734 PMCid:PMC1838910

Williams G.C., Lindo K.G. 1997. A review of the octocorallian genus Leptogorgia (Anthozoa: Gorgoniidae) in the Indian Ocean and Subantarctic, with description of a new species and comparisons with related taxa. Proc. Calif. Acad. Sci. 49: 499-521.

Williams G.C. Chen J.Y. 2012. Resurrection of the octocorallian genus Antillogorgia for Caribbean species previously assigned to Pseudopterogorgia, and a taxonomic assessment of the relationship of these genera with Leptogorgia (Cnidaria, Anthozoa, Gorgoniidae). Zootaxa 3505: 39-52.

Winkler I.S., Blaschke J.D., Davis D.J., et al. 2015. Explosive radiation or uninformative genes? Origin and early diversification of tachinid flies (Diptera: Tachinidae). Mol. Phylogenet. Evol. 88: 38-54. https://doi.org/10.1016/j.ympev.2015.03.021 PMid:25841383

Wirshing H.H., Baker A.C. 2015. Molecular and morphological species boundaries in the gorgonian octocoral genus Pterogorgia (Octocorallia: Gorgoniidae). PLoS one 10: e0133517.

Yasuda N., Taquet C., Nagai S., et al. 2015. Genetic diversity, paraphyly and incomplete lineage sorting of mtDNA, ITS2 and microsatellite flanking region in closely related Heliopora species (Octocorallia). Mol. Phylogenet. Evol. 93: 161-171.

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2017-06-30

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Soler-Hurtado MM, Megina C, Machordom A, López-González PJ. Foxed intra- and interspecific differentiation in Leptogorgia (Octocorallia: Gorgoniidae). A description of a new species based on multiple sources of evidence. Sci. mar. [Internet]. 2017Jun.30 [cited 2024Mar.28];81(2):147-5. Available from: https://scientiamarina.revistas.csic.es/index.php/scientiamarina/article/view/1707

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