Psychedelics sea slugsObservations on colour ontogeny in two nudibranch species from the genus Nembrotha (Doridina: Polyceridae)

  1. Pola, Marta 1
  2. Tibiriçá, Yara 2
  3. Cervera, Juan Lucas 3
  1. 1 Departamento de Biología, Facultad de Ciencias, Universidad Autónoma de Madrid - Centro de Investigación en Biodiversidad y Cambio Global (CIBC-UAM)
  2. 2 Stazione Zoologica Anton Dohrn, Italy. Res. Marina Biology Station of Inhaca - Departamento de Biología, Facultad de Ciencias del Mar y Ambientales, Campus de Excelencia Internacional del Mar (CEI·MAR), Universidad de Cádiz
  3. 3 Departamento de Biología, Facultad de Ciencias del Mar y Ambientales, Campus de Excelencia Internacional del Mar (CEI·MAR), Universidad de Cádiz - Instituto Universitario de Investigación Marina (INMAR), Campus de Excelencia Internacional del Mar (CEI•MAR), Universidad de Cádiz
Revista:
Scientia Marina

ISSN: 0214-8358

Año de publicación: 2023

Volumen: 87

Número: 3

Tipo: Artículo

DOI: 10.3989/SCIMAR.05371.072 DIALNET GOOGLE SCHOLAR lock_openAcceso abierto editor

Otras publicaciones en: Scientia Marina

Resumen

En las últimas décadas, gracias al uso de la taxonomía integrada, el reconocimiento tradicional de una especie basado en la observación y la variación del patrón de color en los nudibranquios se ha vuelto cada vez más cuestionado, principalmente debido a la presencia de complejos de especies crípticas y pseudocrípticas. Por lo tanto, los individuos con el mismo patrón de color pueden ser genéticamente idénticos, pero los individuos con diferentes patrones de color también pueden ser genéticamente idénticos y, en cambio, esta variación puede representar diferentes etapas de la vida. Pero las cosas pueden complicarse aún más. ¿Qué sucede cuando la misma especie cambia radicalmente su patrón de color a medida que envejece? Aquí presentamos dos ejemplos extraordinarios en especies del género Nembrotha basados en observaciones de laboratorio. Se recolectaron ejemplares de Nembrotha livingstonei Allan, 1933 y Nembrotha yonowae Goethel and Debelius, 1992 en Mozambique y se mantuvieron en cautiverio mientras fue posible alimentarlos. Los resultados mostraron que los patrones de color en ambas especies cambiaron con el tiempo y que este cambio estaba relacionado con la dieta. Además, el análisis de delimitación de especies y la comparación de las distancias por pares no corregidas de COI de ejemplares examinados de Mozambique y otros descargados de GenBank confirmaron que N. yonowae Goether y Debelius, 1992 es un sinónimo menor de N. cristata Bergh, 1877. Estudios similares con observaciones de laboratorio son necesarios en otras especies del género, ya que se describieron en función de una coloración diferente, pero la taxonomía integrada puede mostrar resultados diferentes.

Referencias bibliográficas

  • Alqudah A., Saad S., Susanti D., et al. 2016. Observations on nudibranch behaviour patterns under laboratory conditions. J. Teknol. 78: 167-171. https://doi.org/10.11113/.v78.6639
  • Anderson J. 2022. Maldives nudibranchs and Others Sea Slugs. A photographic identification guide. Available at http://www.nudibranch.org/iBooks/identification%20guides.html.
  • Ávila C. 1996. The growth of Peltodoris atromaculata Bergh, 1880 (Gastropoda: Nudibranchia) in the laboratory. J. Molluscan Stud. 62: 151-157. https://doi.org/10.1093/mollus/62.2.151
  • Bandaranayake W.M. 2006. The nature and role of pigments of marine invertebrates. Nat. Prod. Rep. 23: 223-255. https://doi.org/10.1039/b307612c PMid:16572229
  • Bergh L. S. R. 1887. Malacologische Untersuchungen, In: C. Semper (ed) Reisen im Archipel der Philippinen. Zweiter Theil, Wissenchaftliche Resultate, 2: 429-494.
  • Bickford D., Lohman D.J., Sodhi N.S., et al. 2007. Cryptic species as a window on diversity and conservation. Trends Ecol. Evol. 22: 148-155. https://doi.org/10.1016/j.tree.2006.11.004 PMid:17129636
  • Booth C.L. 1990. Evolutionary significance of ontogenetic colour change in animals. Biol. J. Linn. Soc. 40: 125-163. https://doi.org/10.1111/j.1095-8312.1990.tb01973.x
  • Bornancin L., Bonnard I., Mills S.C., Banaigs B. 2017. Chemical mediation as a structuring element in marine gastropod predator-prey interactions. Nat. Prod. Rep. 34: 644-676. https://doi.org/10.1039/C6NP00097E PMid:28466897
  • Calado R., Dinis M.T. 2005. Nudibranchs in the marine Aquarium trade system. Portugala 5: 17.
  • Carmona L., Lei B.R., Pola M., et al. 2014. Untangling the Spurilla neapolitana (Delle Chiaje, 1841) species complex: a review of the genus Spurilla Bergh, 1864 (Mollusca: Nudibranchia: Aeolidiidae). Zool. J. Linn. Soc. 170: 132-154. https://doi.org/10.1111/zoj.12098
  • Coleman N. 2008. Nudibranchs enciclopedia, catalogue of Asia/Indo-Pacific sea slugs. Neville Coleman's Underwater Geographic Pty Ltd. 416 pp.
  • Córdoba González D., Enguidanos A., Valdés Á., Ballesteros M. 2022. Changing feeding habits and ontogenetic dimorphism in juveniles and adults Aplysia punctata (Cuvier, 1803) (Mollusca, Gastropoda, Heterobranchia) in the Mediterranean Sea. Mediterr. Mar. Sci. 23. https://doi.org/10.12681/mms.29735
  • De Bruyn R. A., Gosselin L. A. 2014. Prevalence of ontogenetic changes in colour brightness among benthic invertebrates and their association with microhabitat shifts. Mar. Ecol. Prog. Ser. 498: 147-159. https://doi.org/10.3354/meps10626
  • Debelius H., Kuiter R. 2007. Nudibranchs of the world. IKAN-Unterwasserarchiv. Frankfurt, Germany.
  • Dean L. J., Prinsep M. R. 2017. The chemistry and chemical ecology of nudibranchs. Nat. Prod. Rep. 34: 1359-1390. https://doi.org/10.1039/C7NP00041C PMid:29135002
  • Dionisio G., Rosa R., Costa Leal M., et al. 2013. Beauties and beasts: a portrait of sea slugs aquaculture. Aquac. 408-409: 1-14. https://doi.org/10.1016/j.aquaculture.2013.04.033
  • Fisch K.M., Hertzer C., Böhringer N., et al. 2017. The potential of Indonesian heterobranchs found around Bunaken Island for the production of bioactive compounds. Mar. Drugs. 15: 384. https://doi.org/10.3390/md15120384 PMid:29215579 PMCid:PMC5742844
  • Folmer R.O., Black M., Hoeh W., et al. 1994. DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol. Marine Biol. Biotechnol. 3: 294-299.
  • Goethel H., Debelius H. 1992. Nacktschnecken der Maldiven, mit der Beschreibung einer neuen Art. DATZ (Die Aquarien- und Terrarienzeitschrift), 8: 512-519.
  • Goodheart J., Valdés Á. 2013. Re-evaluation of the Doriopsilla areolata Bergh, 1880 (Mollusca: Opisthobranchia) subspecies complex in the eastern Atlantic Ocean and its relationship to South African Doriopsilla miniate (Alder and Hancock, 1864) based on molecular data. Mar. Biodivers. 43: 113-120. https://doi.org/10.1007/s12526-012-0136-1
  • Gosliner T.M. 1980. The systematics of the Aeolidacea (Nudibranchia: Mollusca) of the Hawaiian Islands, with description of two new species. Pac. Sci. 33: 37-77.
  • Gosliner T.M., Valdés Á., Behrens D.W. 2018. Nudibranchs and Sea Slug Identification Indo-Pacific. New World Publications, Inc., Jacksonville, Florida, 451 pp.
  • Hallas J.M., Chichvarkhin A., Gosliner T.M. 2017. Aligning evidence: concerns regarding multiple sequence alignments in estimating the phylogeny of the Nudibranchia suborder Doridina. R. Soc. Open Sci. 4: 171095. https://doi.org/10.1098/rsos.171095 PMid:29134101 PMCid:PMC5666284
  • Hultgren K.M., Mittelstaedt H. 2015. Color change in a marine isopod is adaptive in reducing predation. Curr. Zool. 61: 739-748. https://doi.org/10.1093/czoolo/61.4.739
  • Human P., Deloach N. 2010. Reef Creature Identification Tropical Pacific. New World Publication, inc. ISBN, 978-1878348.
  • Karuso P., Scheuer P.J. 2002. Natural products from three nudibranchs: Nembrotha kubaryana, Hypselodoris infucata and Chromodoris petechialis. Molecules. 7: 1-6. https://doi.org/10.3390/70100001-rev PMCid:PMC6146475
  • Kearse M., Moir R., Wilson A., et al. 2012. Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28: 1647-1649. https://doi.org/10.1093/bioinformatics/bts199 PMid:22543367 PMCid:PMC3371832
  • Knutson V.L., Gosliner T.M. 2022. The first phylogenetic and species delimitation study of the nudibranch genus Gymnodoris reveals high species diversity (Gastropoda: Nudibranchia). Mol. Phylogenet. Evol. 171: 107470. https://doi.org/10.1016/j.ympev.2022.107470 PMid:35358690
  • Korshunova T.A., Driessen F.M., Picton B.E., Martynov A.V. 2021. The multilevel organismal diversity approach deciphers difficult to distinguish nudibranch species complex. Sci. Rep. 11: 1-22. https://doi.org/10.1038/s41598-021-94863-5 PMid:34526521 PMCid:PMC8443629
  • Kraus F., Allison A. 2009. A remarkable ontogenetic change in color pattern in a new species of Oreophryne (Anura: Microhylidae) from Papua New Guinea. Copeia 4: 690-697. https://doi.org/10.1643/CH-09-015
  • Kumar S., Stecher G., Tamura K. 2016. MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol. Biol. Evol. 33: 1870-1874. https://doi.org/10.1093/molbev/msw054 PMid:27004904 PMCid:PMC8210823
  • Layton K.K., Gosliner T.M., Wilson, N.G. 2018. Flexible colour patterns obscure identification and mimicry in Indo-Pacific Chromodoris nudibranchs (Gastropoda: Chromodorididae). Mol. Phylogenet. Evol. 124: 27-36. https://doi.org/10.1016/j.ympev.2018.02.008 PMid:29476907
  • Mann D. G., Evans K. M. 2008. The species concept and cryptic diversity. In: Moestrup Ø et al. (eds). Proceedings of the 12th International Conference on Harmful Algae. International Society for the Study of Harmful Algae and Intergovernmental Oceanographic Commission of UNESCO.
  • Miller M.A., Pfeiffer W., Schwartz T. 2010. Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In: Proceedings of the Gateway Computing Environments Workshop (GCE), pp 1-8. https://doi.org/10.1109/GCE.2010.5676129 https://doi.org/10.1109/GCE.2010.5676129
  • MolluscaBase eds. 2022. MolluscaBase. Nembrotha Bergh, 1877. Accessed through: World Register of Marine Species on 2022-10-13 at: https://www.marinespecies.org/aphia.php?p=taxdetailsandid=456473
  • Nakano R. 2004. Opisthobranchs of Japan Islands. Rutles, Inc. 304 pp.
  • Nakano R. 2018. Field Guide to Sea Slugs and Nudibranchs of Japan. Bun-ichi Co. Ltd. Tokyo, Japan, 544 pp.
  • Ono A. 1999. Opisthobranchs of Kerama Islands TBS-Britannica Co., Ltd. Tokyo, Japan, 184 pp.
  • Ortea J., Valdés A., García-Gómez J.C. 1996. Revisión de las especies atlánticas de la familia Chromodorididae (Mollusca: Nudibranchia) de grupo cromático azul. Avicennia Suppl. 1: 1-165.
  • Padula V., Araújo A. K., Matthews-Cascon H., Schrödl M. 2014. Is the Mediterranean nudibranch Cratena peregrina (Gmelin, 1791) present on the Brazilian coast? Integrative species delimitation and description of Cratena minor n. sp. J. Molluscan Stud. 80: 575-584. https://doi.org/10.1093/mollus/eyu052
  • Padula V., Bahía J., Stöger I., et al. 2016. A test of color-based taxonomy in nudibranchs: molecular phylogeny and species delimitation of the Felimida clenchi (Mollusca: Chromodorididae) species complex. Mol. Phylogenet. Evol. 103: 215-229. https://doi.org/10.1016/j.ympev.2016.07.019 PMid:27444708
  • Paul V. J., Lindquist N., Fenical W. 1990. Chemical defenses of the tropical ascidian Atapozoa sp. and its nudibranch predators Nembrotha spp. Mar. Ecol. Prog. Ser.: 109-118. https://doi.org/10.3354/meps059109
  • Paz-Sedano S., Martín Álvarez J. F., Gosliner T.M., Pola M. 2022. Reassessing North Eastern Atlantic Mediterranean species of Trapania (Mollusca, Nudibranchia). Zool. Scr. 51: 447-459. https://doi.org/10.1111/zsc.12536
  • Pola M., Cervera J.L., Gosliner T.M. 2006. Taxonomic revision and phylogenetic analysis of the genus Tambja Burn, 1962 (Mollusca, Nudibranchia, Polyceridae). Zool. Scr. 35: 491-530. https://doi.org/10.1111/j.1463-6409.2006.00241.x
  • Pola M., Cervera J.L., Gosliner T.M. 2007. Phylogenetic relationships of Nembrothinae (Mollusca: Doridacea: Polyceridae) inferred from morphology and mitochondrial DNA. Mol. Phylogenet. Evol. 43: 726-742. https://doi.org/10.1016/j.ympev.2007.02.003 PMid:17470399
  • Pola M., Cervera J.L., Gosliner T.M. 2008. Revision of the Indo-Pacific genus Nembrotha (Nudibranchia: Dorididae: Polyceridae), with a description of two new species. Sci. Mar. 72: 145-183. https://doi.org/10.3989/scimar.2008.72n1145
  • Puillandre N., Brouillet S., Achaz G. 2021. ASAP: assemble species by automatic partitioning. Mol. Ecol. Resour. 21: 609-620. https://doi.org/10.1111/1755-0998.13281 PMid:33058550
  • Rudman W.B. 1999-2005. Sea Slug Forum. Australian Museum, Sydney. Available from http://www.seaslugforum.net.
  • Rudman W.B. 2007. Comment on Nembrotha cristata feeding from Raja Ampat by Mike Krampf. [Message in] Sea Slug Forum. Australian Museum, Sydney. Available from http://www.seaslugforum.net/find/19177.
  • Sørensen C., Rauch C, Pola M., Malaquias M.A.E. 2020. Integrative taxonomy reveals a cryptic species of the nudibranch genus Polycera (Polyceridae) in Europeans waters. J. Mar. Biol. Assoc. U.K. 100: 733-752. https://doi.org/10.1017/S0025315420000612
  • Tibiriçá Y., Pola M., Cervera J.L. 2017. Astonishing diversity revealed: an annotated and illustrated inventory of Nudipleura (Gastropoda: Heterobranchia) from Mozambique. Zootaxa 4359: 001-133. https://doi.org/10.11646/zootaxa.4359.1.1 PMid:29245453
  • Tibiriçá Y., Pola M., Cervera J.L. 2018. Systematics of the genus Halgerda Bergh, 1880 (Heterobranchia: Nudibranchia) of Mozambique with descriptions of six new species. Invertebr. Syst. 32: 1388-1421. https://doi.org/10.1071/IS17095
  • Toms J.A., Pola M., von der Heyden S., Gosliner T.M. 2021. Disentangling species of the genus Limacia O.F. Müller, 1781 from southern Africa and Europe using integrative taxonomical methods, with the description of four new species. Mar. Biodivers. 51: 1-31. https://doi.org/10.1007/s12526-020-01125-0
  • Tonozuka T. 2003. Opisthobranchs of Bali and Indonesia, Hankyu Communications Co., Ltd., 165 pp.
  • Valdés Á., Ornelas-Gatdula E., Dupont A. 2013. Color pattern variation in a shallow-water species of opisthobranch mollusc. Biol. Bull. 224: 35-46. https://doi.org/10.1086/BBLv224n1p35 PMid:23493507
  • Wells F., Clayton W.B. 1993. Sea slugs and their relatives of Western Australia. Western Australia Museum: 1-184 pp.
  • Wilson D., Heinsohn R., Endler J.A. 2007. The adaptative significance of ontogenetic colour change in a tropical python. Biol. Lett. 3: 40-43. https://doi.org/10.1098/rsbl.2006.0574 PMid:17443961 PMCid:PMC2373822
  • Winters A.E., Green N.F., Wilson N.G., et al. 2017. Stabilizing selection on individual pattern elements of aposematic signals. Proc. Royal Soc. B Biol. Sci. 284(1861): 20170926. https://doi.org/10.1098/rspb.2017.0926 PMid:28835556 PMCid:PMC5577479
  • Winters A.E., Chan W., White A.M., et al. 2022. Weapons or deterrents? Nudibranch molluscs use distinct ecological modes of chemical defence against predators. J. Anim. Ecol. 91: 831-844. https://doi.org/10.1111/1365-2656.13643 PMid:34839542
  • Yonow N. 1994. Opisthobranchs from the Maldive Islands, including descriptions of seven new species (Mollusca: Gastropoda). Revue Française DÁquariologie Herpetologie, 20: 97-130.
  • Yonow N. 2012. Opisthobranchs from the western Indian Ocean, with descriptions of two new species and ten new records (Mollusca, Gastropoda). Zookeys, 197: 1-129. https://doi.org/10.3897/zookeys.197.1728 PMid:22711992 PMCid:PMC3376724