Abstract
Mollusks are a very important component of the invertebrate faunal biodiversity in marine ecosystems. However, knowledge on this (and other groups) is still incomplete. Inventories of fauna are very important tools to learn the biodiversity associated with specific regions and of specific zoological groups. In this paper, I report 103 species of heterobranch mollusks occurring along the Pacific coast of Colombia, including previous peer-reviewed records and new information. Of these, 23 are new records for the Pacific coast of Colombia, and a total of 32 species are registered for the first time in at least one locality along this shore. The most species diverse family is Chromodorididae, followed by Ellobiidae. The most diverse locality is Gorgona Island, closely followed by Malpelo Island. There is still much to learn from this rather isolated region, the northern Pacific coast of the South American continent.
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Angulo-Campillo O, Bertsch H (2013) Marionia kinoi (Nudibranchia: Tritoniidae): a new species from the tropical eastern Pacific. Nautilus (philadelphia) 127:85–89
Appeltans W, Ahyong ST, Anderson G et al (2012) The magnitude of global marine species diversity. Curr Biol 22:2189–2202. https://doi.org/10.1016/j.cub.2012.09.036
Ardila NE, Báez DP, Valdés Á (2007) Babosas y liebres de mar (Mollusca: Gastropoda: Opisthobranchia) de Colombia. Biota Colomb 8:185–197
Báez DP, Ardila N, Valdás Á, Acero PA (2011) Taxonomy and phylogeny of Armina (Gastropoda: Nudibranchia: Arminidae) from the Atlantic and eastern Pacific. J Mar Biol Assoc United Kingdom 91:1107–1121. https://doi.org/10.1017/S0025315410002109
Barber PH, Ablan-Lagman MCA, Ambariyanto A et al (2014) Advancing biodiversity research in developing countries: the need for changing paradigms. Bull Mar Sci 90:187–210. https://doi.org/10.5343/bms.2012.1108
Bazzicalupo E, Crocetta F, Gosliner TM et al (2020) Molecular and morphological systematics of Bursatella leachii de Blainville, 1817 and Stylocheilus striatus Quoy & Gaimard, 1832 reveal cryptic diversity in pantropically distributed taxa (Mollusca: Gastropoda: Heterobranchia). Invertebr Syst 34:535–568. https://doi.org/10.1071/IS19056
Behrens DW, Hermosillo A (2005) Eastern Pacific Nudibranchs: a guide to the Opisthobranchs from Alaska to Central America. Sea Challengers, Monterey, California, USA
Benedetti-Cecchi L (2006) Understanding the consequences of changing biodiversity on rocky shores: how much have we learned from past experiments? J Exp Mar Bio Ecol 338:193–204. https://doi.org/10.1016/j.jembe.2006.06.020
Bertsch H (2020) A history of eastern Pacific marine heterobranch research. Nautilus (philadelphia) 134:71–88
Bertsch H (2019) Biodiversity and natural history of Nudipleura communities (Mollusca, Gastropoda) at Bahía de los Ángeles, Baja California, Mexico. A 30-year study. Geomare Investig Terr y Mar 1:89–136
Bertsch H (2010) Biogeography of northeast Pacific opisthobranchs: comparative faunal province studies between Point Conception, California, USA, and Punta Aguja, Piura, Perú. In: L.J. Rangel-Ruíz, J. Gamboa-Aguilar SLA-W& WMC-S (ed) Perspectivas en Malacología Mexicana. Universidad Juárez Autónoma de Tabasco, La Paz, pp 219–259
Bertsch H (1978) The Chromodoridinae Nudibranchs from the Pacific coast of America - Part III. The Genera Chromolaichma and Mexichromis. The Veliger 21:70–86
Bertsch H (1972) Two additions to the Opisthibranch fauna of the southern Gulf of California. The Veliger 15:103–106
Bertsch H, Ferreira AJ (1974) Four new species of Nudibranchs from Tropical West America. The Veliger 16:343–353
Bouchet P (2006) The magnitude of marine biodiversity. In: Duarte CM (ed) The exploration of marine biodiversity scientific and technological challenges. Fundación BBVA, pp 31–64
Brusca RC, Moore W, Shuster SM (2016) Invertebrates, Third Edit. Sinauer Associates, Inc., Sunderland, Massachusetts, USA
Camacho-Garcia Y, Gosliner TM, Valdés Á (2005) Field guide to the sea slugs of the Tropical Eastern Pacific. California Academy of Sciences, San Francisco
Camacho-García YE, Gosliner TM (2004) A new species of Okenia (Gastropoda: Nudibranchia: Goniodorididae) from the Pacific Coast of Costa Rica. Proc Calif Acad Sci 55:431–438
Camacho-García YE, Gosliner TM (2008) Nudibranch Dorids from the Pacific Coast of Costa Rica with the description of a new species. Bull Mar Sci 83:367–389
Cantera Kintz JR, López de Mesa LÁ, Cuéllar LM, Londoño-Cruz E (2011) Moluscos. In: Cantera Kintz JR, Londoño-Cruz E (eds) Colombia Pacífico: Una visión sobre su Biodiversidad Marina. Programa Editorial Universidad del Valle, Cali, pp 125–200
Cantera K. JR, Rubio R. EA, Borrero FJ, et al (1979) Taxonomía y distribución de los moluscos litorales de la Isla de Gorgona. In: Prahl H, Guhl F, Gröghl M (eds) Gorgona. Universidad de Los Andes, Bogotá, pp 141–168
Carmona L, Lei BR, Pola M et al (2014a) 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
Carmona L, Pola M, Gosliner TM, Cervera JL (2017) Integrative taxonomy and biogeography of the genus Bulbaeolidia (Nudibranchia: Aeolidida). J Molluscan Stud 83:440–450. https://doi.org/10.1093/mollus/eyx027
Carmona L, Pola M, Gosliner TM, Cervera JL (2013) A Tale That Morphology Fails to Tell: A Molecular Phylogeny of Aeolidiidae (Aeolidida, Nudibranchia, Gastropoda). PLoS One 8:e63000. https://doi.org/10.1371/journal.pone.0063000
Carmona L, Pola M, Gosliner TM, Cervera JL (2014) The end of a long controversy: systematics of the genus Limenandra (Mollusca: Nudibranchia: Aeolidiidae). Helgol Mar Res 68:37–48. https://doi.org/10.1007/s10152-013-0367-yAeolidiidae
Cosel R von (1985) Moluscos marinos de la Isla de Gorgona (Costa del Pacífico Colombiana). An del Inst Investig Mar Punta Betin 14:175–257
Costello MJ, Coll M, Danovaro R, et al (2010) A census of marine biodiversity knowledge, resources, and future challenges. PLoS One 5:e121110. https://doi.org/10.1371/journal.pone.0012110
Dinapoli A, Klussmann-Kolb A (2010) The long way to diversity - phylogeny and evolution of the Heterobranchia (Mollusca: Gastropoda). Mol Phylogenet Evol 55:60–76. https://doi.org/10.1016/j.ympev.2009.09.019
Duarte CM (2000) Marine biodiversity and ecosystem services: an elusive link. J Exp Mar Bio Ecol 250:117–131. https://doi.org/10.1016/S0022-0981(00)00194-5
Fisher R, O’Leary RA, Low-Choy S et al (2015) Species richness on coral reefs and the pursuit of convergent global estimates. Curr Biol 25:500–505. https://doi.org/10.1016/j.cub.2014.12.022
Fisch KM, Hertzer C, Böringer N et al (2017) The potential of Indonesian heterobranchs found around Bunaken Island for the production of bioactive compounds. Mar Drugs 15:339–384. https://doi.org/10.3390/md15120384
Foggo A, Attrill MJ et al (2003) Estimating marine species richness: an evaluation of six extrapolative techniques. Mar Ecol Prog Ser 248:15–26
Furfaro G, Vitale F, Licchelli C, Mariottini P (2020) Two seas for one great diversity: Checklist of the marine heterobranchia (Mollusca; Gastropoda) from the Salento Peninsula (South-East Italy). Diversity 12:171. https://doi.org/10.3390/D12050171
Garcia FJ, Troncoso JS (2001) Favorinus elenalexiae, a new species (Opisthobrancha: Aeolidiidae) from the eastern Pacific Ocean. Nautilus (philadelphia) 115:55–61
Gotelli NJ, Colwell RK (2001) Quantifying biodiversity: procedures and pitfalls in the measurement and comparison of species richness. Ecol Lett 4:379–391
Hermosillo A (2006) Ecología de los Opistobranquios (Mollusca) de Bahía de Banderas, Jalisco-Nayarit, México. Universidad de Guadalajara
IDEAM (2019) Pronóstico de Pleamares y Bajamares en la costa Pacífica Colombiana. Bogotá, Colombia
INVEMAR (2020) Informe del Estado de los Ambientes Y Recursos Marinos y costeros de Colombia, Serie de P. Santa Marta
Kaiser KL, Bryce CW (2001) The recent molluscan marine fauna of Isla de Malpelo. Colombia the Festivus 33:158
Kaligis F, Eisenbarth JH, Schillo D et al (2018) Second survey of heterobranch sea slugs (Mollusca, Gastropoda, Heterobranchia) from Bunaken National Park, North Sulawesi, Indonesia - How much do we know after 12 years? Mar Biodivers Rec 11:1–20. https://doi.org/10.1186/s41200-018-0136-3
Keen M (1971) Sea shells of Tropical West America: marine mollusks from Baja California to Peru. Stanford University Press, Stanford, Second
López de Mesa LÁ, Cantera JR (2015) Marine mollusks of Bahía Málaga, Colombia (Tropical Eastern Pacific). Check List 11. https://doi.org/10.15560/11.1.1497
Loreau M, de Mazancourt C (2013) Biodiversity and ecosystem stability: a synthesis of underlying mechanisms. Ecol Lett 16:106–115. https://doi.org/10.1111/ele.12073
Lozano-Cortés D, Londoño-Cruz E, Izquierdo V et al (2012) Checklist of benthonic marine invertebrates from Malaga Bay (Isla Palma and Los Negritos), Colombian Pacific. Check List 8:703. https://doi.org/10.15560/8.4.703
Málikov I, Villegas-Bolaños NL (2005) Construcción de Series de Tiempo de Temperatura Superficial del Mar de las Zonas Homogéneas del Océano Pacífico Colombiano. Boletín Científico CCCP 12:79–93. https://doi.org/10.26640/01213423.12.79_93
Medrano S, Krug PJ, Gosliner TM et al (2019) Systematics of Polybranchia Pease, 1860 (Mollusca: Gastropoda: Sacoglossa) based on molecular and morphological data. Zool J Linn Soc 186:76–115. https://doi.org/10.1093/zoolinnean/zly050
Mittermeier RA, Robles-Gil P, Hoffmann M, et al (2004) Hotspots Revisited: Earth’s Biologically Richest and Most Endangered Terrestrial Ecoregions. CEMEX, Mexico City, Mexico
Mittermeier RA, Turner WR, Larsen FW et al (2011) Global biodiversity conservation: the critical role of hotspots. In: Zachos FE, Habel JC (eds) Biodiversity Hotspots. Distribution and Protection of Conservation Priority Areas. Springer, Berlin, pp 3–22
Mora C, Tittensor DP, Adl S et al (2011) How many species are there on earth and in the ocean? PLoS Biol 9:1–8. https://doi.org/10.1371/journal.pbio.1001127
Naeem S, Loreau M, Inchausti P (2002) Biodiversity and ecosystem functioning: the emergence of a synthetic ecological framework. Biodiversity and ecosystem functioning: Synthesis and Perspectives. Oxford University Press, Oxford, pp 3–17
Nimbs MJ, Smith SDA (2018) Beyond capricornia: Tropical sea slugs (Gastropoda, Heterobranchia) extend their distributions into the Tasman Sea. Diversity 10:99. https://doi.org/10.3390/d10030099
Pimm SL (2012) Biodiversity: not just lots of fish in the sea. Curr Biol 22:R996–R997. https://doi.org/10.1016/j.cub.2012.09.028
Pola M, Cervera JL, Gosliner TM (2005) Review of the systematics of the genus Roboastra Bergh, 1877 (Nudibranchia, Polyceridae, Nembrothinae) with the description of a new species from the Galápagos Islands. Zool J Linn Soc 144:167–189. https://doi.org/10.1111/j.1096-3642.2005.00167.x
Robertson R (1979) Philippia (Psilaxis) radiata: Another Indo-West-Pacific Architectonicid newly found in the Easter Pacific (Colombia). The Veliger 22:191–193
R Core Team (2020) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL https://www.R-project.org/
Rangel-Ch. JO, Arellano-P. H (2004) El Chocó biogeográfico/Costa Pacífica de Colombia. In: Rangel-Che. JO (ed) Colombia Diversidad Biótica IV. Instituto de Ciencias Naturales, Bogotá, pp 39–82
Schubert J, Smith SDA (2020) Sea slugs-"rare in space and time"-But Not Always. Diversity 12:1–14. https://doi.org/10.3390/d12110423
Smith SDA (2005) Rapid assessment of invertebrate biodiversity on rocky shores: where there’s a whelk there’s a way. Biodivers Conserv 14:3565–3576. https://doi.org/10.1007/s10531-004-0828-3
Undap N, Papu A, Schillo D et al (2019) First survey of heterobranch sea slugs (Mollusca, Gastropoda) from the Island Sangihe, North Sulawesi. Indonesia Diversity 11:170. https://doi.org/10.3390/d11090170
Uribe RA, Sepúlveda F, Goddard JHR, Valdés Á (2018) Integrative systematics of the genus Limacia O. F. Müller, 1781 (Gastropoda, Heterobranchia, Nudibranchia, Polyceridae) in the Eastern Pacific. Mar Biodivers 48:1815–1832. https://doi.org/10.1007/s12526-017-0676-5
Valdés Á (2002) A phylogenetic analysis and systematic revision of the cryptobranch dorids (Mollusca, Nudibranchia, Anthobranchia). Zool J Linn Soc 136:535–636. https://doi.org/10.1046/j.1096-3642.2002.00039.x
Valdés Á, Breslau E, Padula V et al (2018) Molecular and morphological systematics of Dolabrifera Gray, 1847 (Mollusca: Gastropoda: Heterobranchia: Aplysiomorpha). Zool J Linn Soc 184:31–35. https://doi.org/10.1093/zoolinnean/zlx099
Acknowledgements
I am deeply indebted to my friend and colleague Jaime Cantera for his continuing support and encouragement towards the study of nudibranchs and the long talks regarding invertebrate biodiversity in general. He also read and improved this manuscript. I am especially grateful to my biology students at Universidad del Valle that knowing my passion for heterobranch sea slugs continuously pointed me towards these creatures whenever they spotted one. I am also indebted to my university that financially supported all the courses’ field trips. Finally, I want to express my deepest gratitude to my colleagues Maria Fernanda Cardona-Gutierrez, Luz Angela López de Mesa, and especially to Hans Bertsch that critically read, corrected, and enhanced this manuscript. Last but not least, three anonymous reviewers critically assessed the first version of the manuscript, and their contributions were reflected in a big improvement of this paper. This is contribution number 22 from INCIMAR.
Funding
No funding was received for conducting this study in particular; however, Universidad del Valle (Cali, Colombia) financially supported all the courses’ field trips in which most of the records were obtained. Other observations were made during various research projects financed by COLCIENCIAS and Universidad del Valle, grant numbers 1106–405-20155, “Biodiversidad de Estadios de Vida Vulnerable de Organismos Marinos en Bahía Málaga (Pacífico Colombiano) como criterio de conservación: Evaluación de la heterogeneidad de ambientes en la reproducción y reclutamiento,” and 1106–659-44216, “Relación entre las tasas de bioerosión y bioacreción de arrecifes coralinos de la Isla Gorgona, Pacifico colombiano”, and “Evaluación del estado actual de los objetos de conservación faunísticos en Isla Gorgona: una aproximación holística a la valoración ecológica del PNN Gorgona.”
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Londoño-Cruz, E. The contribution of Heterobranchia (Mollusca: Gastropoda) to the biodiversity of the Colombian Tropical Eastern Pacific. Mar. Biodivers. 51, 93 (2021). https://doi.org/10.1007/s12526-021-01230-8
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DOI: https://doi.org/10.1007/s12526-021-01230-8