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Horizontal and vertical distribution of cephalopod paralarvae in the Mesoamerican Barrier Reef System

Published online by Cambridge University Press:  03 September 2020

Gabriela Castillo-Estrada
Affiliation:
Posgrado en Ciencias del Mar y Limnología, Universidad Nacional Autónoma de México, Ciudad Universitaria 3000, 04510 Coyoacán, México El Colegio de la Frontera Sur (CONACyT), Laboratorio de Pesquerías Artesanales, Av. Rancho Polígono 2A, Ciudad Industrial, Lerma, 24500 Campeche, México
Roxana De Silva-Dávila
Affiliation:
Departamento de Plancton y Ecología Marina, Instituto Politécnico Nacional, Centro Interdisciplinario de Ciencias Marinas, Av. IPN s/n, Fracc. Playa Palo de Sta. Rita, La Paz, Baja California Sur 23096, México
Laura Carrillo
Affiliation:
Departamento de Sistemática y Ecología Acuática, El Colegio de la Frontera Sur (CONACyT), Av. Centenario km 5.5, Col. Pacto Obrero, 77014, Chetumal, Quintana Roo, México
Lourdes Vásquez-Yeomans
Affiliation:
Departamento de Sistemática y Ecología Acuática, El Colegio de la Frontera Sur (CONACyT), Av. Centenario km 5.5, Col. Pacto Obrero, 77014, Chetumal, Quintana Roo, México
Claudia A. Silva-Segundo
Affiliation:
Departamento de Ingeniería en Pesquerías, Universidad Autónoma de Baja California Sur, Sur Km 5.5, 23080, La Paz, B.C.S, México
Laura Avilés-Díaz
Affiliation:
El Colegio de la Frontera Sur (CONACyT), Laboratorio de Pesquerías Artesanales, Av. Rancho Polígono 2A, Ciudad Industrial, Lerma, 24500 Campeche, México
Unai Markaida*
Affiliation:
Posgrado en Ciencias del Mar y Limnología, Universidad Nacional Autónoma de México, Ciudad Universitaria 3000, 04510 Coyoacán, México El Colegio de la Frontera Sur (CONACyT), Laboratorio de Pesquerías Artesanales, Av. Rancho Polígono 2A, Ciudad Industrial, Lerma, 24500 Campeche, México
*
Author for correspondence: Unai Markaida, E-mail: [email protected]

Abstract

Horizontal and vertical distribution of cephalopod paralarvae (PL) from the Mesoamerican Barrier Reef System (MBRS) in the Western Caribbean was studied during two oceanographic cruises in 2006 and 2007. A total of 1034 PL belonging to 12 families, 22 genera, 24 species, 5 morphotypes and a species complex were identified. Abralia redfieldi, Onychoteuthis banksii and Ornithoteuthis antillarum were the most abundant taxa. The taxonomic identification from these three species was corroborated with DNA barcoding (99.8–100% of similarity). Paralarvae of Octopus insularis were reported for the first time in the wild. Most PL occupied the Caribbean Surface Water mass in the 0–25 m depth stratum. Largest paralarval abundances were related to local oceanographic features favouring retention such as the Honduras Gyre and Cozumel eddy. No day-night differences were found in PL abundance, although Abralia redfieldi showed evidence of diel vertical migration. Distribution of PL in epipelagic waters of the MBRS was probably related to ontogenetic migration, hydrographic features of meso and subscale, and to the circulation regimes dominated by the Yucatan Current. The MBRS represents an important dispersion area for PL, potentially connecting a species-rich Caribbean community with the Gulf of Mexico and Florida waters.

Type
Research Article
Copyright
Copyright © Marine Biological Association of the United Kingdom 2020

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References

Aceves-Medina, G, De Silva-Dávila, R, Cruz-Estudillo, I, Durazo, R and Avendaño-Ibarra, R (2017) Influence of the oceanographic dynamic in size distribution of cephalopod paralarvae in the southern Mexican Pacific Ocean (rainy seasons 2007 and 2008). Latin American Journal of Aquatic Research 45, 356369.10.3856/vol45-issue2-fulltext-11CrossRefGoogle Scholar
Adams, CL (1997) Developmental Taxonomy and Distribution of Paralarval Squids from the Florida Current (MS thesis). Florida Institute of Technology, Melbourne, FL, USA.Google Scholar
Arkhipkin, AI, Laptikhovsky, VV, Nigmatullin, C, Bespyatykh, AB and Murzov, SA (1998) Growth, reproduction and feeding of the tropical squid Ornithoteuthis antillarum (Cephalopoda, Ommastrephidae) from the central-east Atlantic. Scientia Marina 62, 273288.10.3989/scimar.1998.62n3273CrossRefGoogle Scholar
Bolstad, K (2010) Systematics of the Onychoteuthidae Gray, 1847 (Cephalopoda: Oegopsida). Zootaxa 2696, 1186.10.11646/zootaxa.2696.1.1CrossRefGoogle Scholar
Bower, JR and Takagi, S (2004) Summer vertical distribution of paralarval gonatid squids in the northeast Pacific. Journal of Plankton Research 26, 851857.Google Scholar
Boyle, P and Rodhouse, P (2005) Cephalopods: Ecology and Fisheries. Oxford: Blackwell Publishing.10.1002/9780470995310CrossRefGoogle Scholar
Cairns, SD (1976) Cephalopods collected in the Straits of Florida by the R/V Gerda. Bulletin of Marine Science 26, 233272.Google Scholar
Canto-García, AA, Goldstein, JS, Sosa-Cordero, E and Carrillo, L (2016) Distribution and abundance of Panulirus spp. phyllosomas off the Mexican Caribbean coast. Bulletin of Marine Science 92, 207227.10.5343/bms.2015.1015CrossRefGoogle Scholar
Carrillo, L, Johns, EM, Smith, RH, Lamkin, JT and Largier, JL (2015) Pathways and hydrography in the Mesoamerican Barrier Reef System. Part 1: circulation. Continental Shelf Research 109, 164176.10.1016/j.csr.2015.09.014CrossRefGoogle Scholar
Carrillo, L, Johns, EM, Smith, RH, Lamkin, JT and Largier, JL (2016) Pathways and hydrography in the Mesoamerican Barrier Reef System. Part 2: water masses and thermohaline structure. Continental Shelf Research 120, 4158.Google Scholar
Carrillo, L, Lamkin, JT, Johns, EM, Vásquez-Yeomans, L, Sosa-Cordero, F, Malca, ER, Smith, H and Gerard, T (2017) Linking oceanographic processes and marine resources in the western Caribbean Sea Large Marine Ecosystem Subarea. Environmental Development 22, 8496.10.1016/j.envdev.2017.01.004CrossRefGoogle Scholar
De Silva-Dávila, R (2013) Paralarvas de cefalópodos en el Golfo de California, México (PhD thesis). Universidad de Guadalajara–CUCSUR, San Patricio Melaque, Mexico.Google Scholar
De Silva-Dávila, R, Franco-Gordo, C, Hochberg, FG, Godínez-Domínguez, E, Avendaño-Ibarra, R, Gómez-Gutiérrez, J and Robinson, CJ (2015) Cephalopod paralarval assemblages in the Gulf of California during 2004–2007. Marine Ecology Progress Series 520, 123141.10.3354/meps11074CrossRefGoogle Scholar
Díaz, JM, Ardila, N and Gracia, N (2000) Calamares y pulpos (Mollusca: Cephalopoda) del Mar Caribe Colombiano. Biota Colombiana 1, 195201.Google Scholar
Diekmann, R and Piatkowski, U (2002) Early life stages of cephalopods in the Sargasso Sea: distribution and diversity relative to hydrographic conditions. Marine Biology 141, 123130.Google Scholar
Diekmann, R, Nellen, W and Piatkowski, U (2006) A multivariate analysis of larval fish and paralarval cephalopod assemblages at Great Meteor Seamount. Deep-Sea Research I 53, 16351657.Google Scholar
Downey-Breedt, NJ, Roberts, MJ, Sauer, WHH and Chang, N (2016) Modelling transport of inshore and deep-spawned chokka squid (Loligo reynaudi) paralarvae off South Africa: the potential contribution of deep spawning to recruitment. Fisheries Oceanography 25, 2843.Google Scholar
Elías-Gutiérrez, M, Valdez-Moreno, M, Topan, J, Young, MR and Cohuo-Colli, JA (2018) Improved protocols to accelerate the assembly of DNA barcode reference libraries for freshwater zooplankton. Ecology and Evolution 8, 30023018.10.1002/ece3.3742CrossRefGoogle ScholarPubMed
Erickson, C, Roper, CFE and Vecchione, M (2017) Variability of paralarval-squid occurrence in meter-net tows from East of Florida, USA. Southeastern Naturalist 16, 629642.10.1656/058.016.0411CrossRefGoogle Scholar
Goldman, DA (1993) Distribution of cephalopod paralarvae across the Florida Current front in the Florida Keys: preliminary results. Revista de Biología Tropical 41, 3134.Google Scholar
Goldman, DA and McGowan, MF (1991) Distribution and abundance of ommastrephid squid paralarvae off the Florida Keys in August 1989. Bulletin of Marine Science 49, 614622.Google Scholar
Gracia, A, Ardila, NE and Díaz, JM (2002) Cephalopods (Mollusca: Cephalopoda) of the Upper Colombian Caribbean shelf. Biological Investigations of Marine Coasts 31, 219238.Google Scholar
Haimovici, M, Piatkowski, U and Aguiar dos Santos, R (2002) Cephalopod paralarvae around tropical seamounts and oceanic islands of the northeastern coast of Brazil. Bulletin of Marine Science 71, 313330.Google Scholar
Ichii, T, Mahapatra, K, Sakai, M, Inagake, D and Okada, Y (2004) Differing body size between the autumn and the winter-spring cohorts of neon flying squid (Ommastrephes bartramii) related to the oceanographic regime in the North Pacific: a hypothesis. Fisheries Oceanography 13, 295309.10.1111/j.1365-2419.2004.00293.xCrossRefGoogle Scholar
Jereb, P and Roper, CFE (eds) (2010) Cephalopods of the World. An Annotated and Illustrated Catalogue of Cephalopod Species Known to Date, vol. 2. Myopsid and Oegopsid Squids. FAO Species Catalogue for Fishery Purposes, No. 4, Vol. 2. Rome: FAO, pp. 1605.Google Scholar
Judkins, HL, Vecchione, M, Roper, CFE and Torres, J (2010) Cephalopod species richness in the wider Caribbean region. ICES Journal of Marine Science 67, 13921400.Google Scholar
Judkins, HL, Vecchione, M, Cook, A and Sutton, T (2016) Diversity of midwater cephalopods in the northern Gulf of Mexico: comparison of two collecting methods. Marine Biodiversity 47, 647657.10.1007/s12526-016-0597-8CrossRefGoogle Scholar
Kearse, M, Moir, R, Wilson, A, Stone-Havas, S, Cheung, M, Sturrock, S, Buxton, S, Cooper, A, Markowitz, S, Duran, C, Thierer, T, Ashton, B, Meintjes, P and Drummond, A (2012) Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics (Oxford, England) 28, 16471649.10.1093/bioinformatics/bts199CrossRefGoogle ScholarPubMed
Kumar, S, Stecher, G and Tamura, K (2016) MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets. Molecular Biology and Evolution 33, 18701874.10.1093/molbev/msw054CrossRefGoogle ScholarPubMed
Lenz, TM, Elias, NH, Leite, TS and Vidal, EAG (2015) First description of the eggs and paralarvae of the tropical octopus, Octopus insularis, under culture conditions. American Malacological Bulletin 33, 101109.10.4003/006.033.0115CrossRefGoogle Scholar
Lima, FD, Berbel-Filho, WM, Leite, TS, Rosas, C and Lima, SM (2017) Occurrence of Octopus insularis Leite and Haimovici, 2008 in the Tropical Northwestern Atlantic and implications of species misidentification to octopus fisheries management. Marine Biodiversity 47, 723734.10.1007/s12526-017-0638-yCrossRefGoogle Scholar
Martínez, S, Carrillo, L and Marinone, SG (2019) Potential connectivity between marine protected areas in the Mesoamerican Reef for two species of virtual fish larvae: Lutjanus analis and Epinephelus striatus. Ecological Indicators 102, 1020.10.1016/j.ecolind.2019.02.027CrossRefGoogle Scholar
Martínez, S, Carrillo, L, Sosa-Cordero, E, Vásquez-Yeomans, L, Marinone, SG, and Gasca, R (2020) Retention and dispersion of virtual fish larvae in the Mesoamerican Reef. Regional Studies in Marine Science 37, 101350. https://doi.org/10.1016/j.rsma.2020.101350.CrossRefGoogle Scholar
Muhling, BA, Smith, RH, Vásquez-Yeomans, L, Lamkin, JT, Johns, EM, Carrillo, L, Sosa-Cordero, E and Malca, E (2013) Larval reef fish assemblages and mesoscale oceanographic structure along the Mesoamerican Barrier Reef System. Fisheries Oceanography 22, 409428.10.1111/fog.12031CrossRefGoogle Scholar
Nesis, KN (1975) Cephalopods of the American Mediterranean Sea. Trudy Instituta Okeanologii Akademiya Nauk SSSR 100, 259288. [In Russian]. In Sweeney M (ed.), English Translations of Selected Publications on Cephalopods by Kir N. Nesis. Smithsonian Institution Libraries 1, 319–358.Google Scholar
Nesis, KN (1979) Squid larvae of the family Ommastrephidae (Cephalopoda). Zoologicheskii Zhurnal 58, 1730 [In Russian]. In Sweeney M (ed.), English Translations of Selected Publications on Cephalopods by Kir N. Nesis. Smithsonian Institution Libraries 1, 519–536.Google Scholar
Parra-Flores, A and Gasca, R (2009) Distribution of pteropods (Mollusca: Gastropoda: Thecosomata) in surface waters (0–100 m) of the Western Caribbean Sea (winter, 2007). Revista de Biología Marina y Oceanografía 44, 647662.10.4067/S0718-19572009000300011CrossRefGoogle Scholar
Passarella, KC (1990) Oceanic Cephalopod Assemblage in the Eastern Gulf of Mexico (MS thesis). University of South Florida, St. Petersburg, FL, USA.Google Scholar
Roberts, MJ and van den Berg, M (2002) Recruitment variability of chokka squid (Loligo vulgaris reynaudii) – role of currents on the Agulhas Bank (South Africa) in paralarvae distribution and food abundance. Bulletin of Marine Science 71, 691710.Google Scholar
Roberts, CM, McClean, CJ, Veron, JEN, Hawkins, JP, Allen, GR, McAllister, DE, Mittermeier, CG, Schueler, FW, Spalding, M, Wells, F, Vynne, C and Werner, TB (2002) Marine biodiversity hotspots and conservation priorities for tropical reefs. Science (New York, N.Y.) 295, 12801284.10.1126/science.1067728CrossRefGoogle ScholarPubMed
Roper, CFE and Lu, CC (1979) Rhynchoteuthion larvae of ommastrephid squids of the western North Atlantic, with the first description of larvae and juveniles of Illex illecebrosus. Proceedings of the Biological Society of Washington 91, 10391059.Google Scholar
Roper, CFE and Young, RE (1975) Vertical distribution of pelagic cephalopods. Smithsonian Contributions to Zoology 209, 51 pp.Google Scholar
Roper, CFE, Gutierrez, A and Vecchione, M (2015) Paralarval octopods of the Florida Current. Journal of Natural History 49, 12811304.10.1080/00222933.2013.802046CrossRefGoogle Scholar
Roura, Á, Álvarez-Salgado, XA, González, AF, Gregori, M, Rosón, G, Otero, J and Guerra, Á (2016) Life strategies of cephalopod paralarvae in a coastal upwelling system (NW Iberian Peninsula): insights from zooplankton community and spatio-temporal analyses. Fisheries Oceanography 25, 241258.10.1111/fog.12151CrossRefGoogle Scholar
Sauer, WHH, Gleadall, IG, Downey-Breedt, N, Doubleday, Z, Gillespie, G, Haimovici, M, Ibáñez, CM, Katugin, ON, Leporati, S, Lipinski, M, Markaida, U, Ramos, JE, Rosa, R, Villanueva, R, Arguelles, J, Briceño, FA, Carrasco, SA, Che, LJ, Chen, CS, Cisneros, R, Conners, E, Crespi-Abril, AC, Kulik, VV, Drobyazin, EN, Emery, T, Fernández-Álvarez, FA, Furuya, H, González, LW, Gough, C, Krishnan, P, Kumar, B, Leite, T, Lu, CC, Mohamed, KS, Nabhitabhata, J, Noro, K, Petchkamnerd, J, Putra, D, Rocliffe, S, Sajikumar, KK, Sakaguchi, H, Samuel, D, Sasikumar, G, Wada, T, Zheng, X, Tian, Y, Pang, Y, Yamrungrueng, A and Pecl, G (2019) World Octopus Fisheries. Reviews in Fisheries Science & Aquaculture. https://doi.org/10.1080/23308249.2019.1680603.Google Scholar
Shea, EK and Vecchione, M (2010) Ontogenic changes in diel vertical migration patterns compared with known allometric changes in three mesopelagic squid species suggest an expanded definition of a paralarva. ICES Journal of Marine Science 67, 14361443.10.1093/icesjms/fsq104CrossRefGoogle Scholar
Sweeney, MJ, Roper, CFE, Mangold, KM, Clarke, MR and Boletzky, SV (1992) “Larval” and juvenile cephalopods: a manual for their identification. Smithsonian Contributions to Zoology 513, 1282.Google Scholar
Thompson, JD, Higgins, DG and Gibson, TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position specific gap penalties and weight matrix choice. Nucleic Acids Research 22, 46734680.10.1093/nar/22.22.4673CrossRefGoogle ScholarPubMed
Tsuchiya, K (2009) Abralia grimpei Voss 1958. The Tree of Life Web Project. http://tolweb.org/Abralia_grimpei/19659/2009.07.26 (Accessed 5 May 2020).Google Scholar
Vecchione, M (1987) Juvenile ecology. In Boyle PR (ed.), Cephalopod Life Cycles, 2. London: Academic Press, pp. 6184.Google Scholar
Vecchione, M, Roper, CFE, Sweeney, MJ and Lu, CC (2001) Distribution, relative abundance and developmental morphology of paralarval cephalopods in the western North Atlantic Ocean. NOAA Technical Report NMFS 152, 154.Google Scholar
Xavier, JC, Allcock A, L, Cherel, Y, Lipinski, MR, Pierce, GJ, Rodhouse, PGK, Rosa, R, Shea, EK, Strugnell, JM, Vidal, EAG, Villanueva, R and Ziegleret, A (2015) Future challenges in cephalopod research. Journal of the Marine Biological Association of the United Kingdom 95, 9991015.10.1017/S0025315414000782CrossRefGoogle Scholar
Young, RE and Harman, RT (1987) Descriptions of the larvae of three species of the Onychoteuthis banksii complex from Hawaiian waters. The Veliger 29, 313321.Google Scholar