Abstract
The taxonomy of squids in the family Loliginidae Lesueur, 1821 is complicated due to their inconsistent descriptions which hamper identification at the species level. In this study, a taxonomic revision of loliginid squids from the northwestern Atlantic was carried out considering morphological, molecular, and morphometric characteristics. Squid were collected in four oceanographic cruises along the coast of Tamaulipas, Gulf of Mexico during the period of 2012 to 2014. Museum (NMNH) specimens (type and non-type material) of the species reported for this area were also considered. The morphological attributes described for each species allowed us to confirm the identity of Doryteuthis pealeii (Lesueur, 1821), Lolliguncula brevis (Blainville, 1823), and males of Doryteuthis pleii (Blainville, 1823); the identification of females of D. pleii and Doryteuthis roperi (Cohen, 1976) (the latter only represented by museum material) was not achieved because of the high interspecific similarity. Three genetic clades were detected with COI sequences associated with each of the three field-collected species that were identified morphologically, including the unidentified females, which were recognized as D. pleii. The morphometry of these three groups was addressed by canonical variate analysis, which supported the interspecific differences. A multivariate analysis of variance was conducted for D. roperi and D. pleii due to their high level of morphological similarity. This analysis indicated significant differences; therefore, it did not allow to confirm if D. roperi is a synonym of D. pleii.
Similar content being viewed by others
References
Addinosoft (2014) XLSTAT software. Version 2014. 3.01. Copyright Addinosoft 1995–2014. Accession date: November 2014. http://www.xlstat.com/es/
Anderson FE (2000) Phylogeny and historical biogeography of the loliginid squids (Mollusca: Cephalopoda) based on mitochondrial DNA sequence data. Mol Phylogenet Evol 15:191–214
Arkhipkin AI, Rodhouse PGK, Pierce GJ, Sauer W, Sakai M, Allcock L, Arguelles J, Bower JR, Castillo G, Ceriola L et al (2015) World squid fisheries. Rev Fish Sci Aquac 23:92–252
Blainville HD (1823) Memoire sur les especes du genre Calmar (Loligo, Lamarck). J Phys Chim Hist Nat Arts 96:116–135
Braga R, Crespi-Abril AC, Van der Molen S, Rodrigues MC, Ortiz N (2017) Analysis of the morphological variation of Doryteuthis sanpaulensis (Cephalopoda: Loliginidae) in Argentinian and Brazilian coastal waters using geometric morphometrics techniques. Mar Biodivers 47(3):755–762
Brakoniecki TF (1986) A generic revision of the family Loliginidae (Cephalopoda; Myopsida) based primarily on the comparative morphology of the hectocotylus. Dissertation, University of Miami
Cohen AC (1976) The systematics and distribution of Loligo (Cephalopoda, Myopsida) in the western North Atlantic, with a description of two new species. Malacologia 15:229–367
DeBose JL, Nevitt GA (2004) Seasonal aggregations of Roper’s inshore squid associated with coral spawning. Oral presentation. USA: 57th Proceedings of the Gulf and Caribbean Fisheries Institute, pp. 1014
DeBose JL, Vecchione M (2005) First documentation of the Roper inshore squid, Loligo roperi (Cohen 1976), in the Gulf of Mexico. Gulf Mex Sci 23:132–135
Elliot NG, Haskard K, Koslow JA (1995) Morphometric analysis of orange roughy (Hoplostethus atlanticus) off the continental slope of southern Australia. J Fish Biol 46:202–220
Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol 3:294–299
Gower JC (1967) A comparison of some methods of cluster analysis. Biometrics 23:623–628
Granados-Amores J (2013) Taxonomía de calamares de la familia Loliginidae en el Pacífico Mexicano [Taxonomy of squids of the family Loliginidae in the Mexican Pacific]. Dissertation, Centro de Investigaciones Biologicas del Noroeste
Granados-Amores J, García-Rodríguez FJ, Hochberg FG, Salinas-Zavala CA (2014) The taxonomy and morphometry of squids in the family Loliginidae (Cephalopoda: Myopsida) from the Pacific coast of Mexico. Am Malacol Bull 32:1–11
Hammer O, Harper DAT, Ryan PD (2001) PAST: paleontological statistics software package for education and data analysis. Paleontol Electron 4(1):1–9
Herke SW, Foltz DW (2002) Phylogeography of two squid (Loligo pealei and L. plei) in the Gulf of Mexico and northwestern Atlantic Ocean. Mar Biol 140:103–115
Jereb P, Vecchione M, Roper CFE (2010) Family Loliginidae. In: Jereb P, Roper CFE (eds) Cephalopods of the world. An annotated and illustrated catalogue of species known to date, Vol. 2: Myopsid and oegopsid squids. FAO Species Catalog for Fishery Purposes, Rome, pp 38–117
Kefferstein W (1866) Kopffüsser: Cephalopoda Cuvier. In: Bronn HG (ed) Die classen un ordnungen des thierreiches: weichthiere (Malacozoa). Leipzig und Heidelberg, 1862–1866. Germany, pp 110–136
Lesueur CA (1821) Description of several new species of cuttlefishes. J Acad Nat Sci Philadelphia 2:86–101
Naef A (1912) Teuthilogische Notizen 4. Die Gattungen der Loliginidae. Zool Anz 39(25):741–745
Roper CFE, Voss GL (1983) Guidelines for taxonomic descriptions of cephalopod species. Mem Mus Natl Vic 44:49–63
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425
Sales JBL, Shaw PW, Haimovici M, Markaida U, Cunha DB, Ready J, Figueiredo-Ready WMB, Schneider H, Sampaio I (2013) New molecular phylogeny of the squids of the family Loliginidae with emphasis on the genus Doryteuthis Naef, 1912: mitochondrial and nuclear sequences indicate the presence of cryptic species in the southern Atlantic Ocean. Mol Phylogenet Evol 68:293–299
Sales JBL, Markaida U, Shaw PW, Haimovici M, Ready JS, Figueredo-Ready WMB, Angioletti F, Carneiro MA, Schneider H, Sampaio I (2014) Molecular phylogeny of the genus Lolliguncula Steenstrup, 1881 based on nuclear and mitochondrial DNA sequences indicates genetic isolation of populations from north and South Atlantic, and the possible presence of further cryptic species. PLoS One 9:1–6
Sales JBL, Rodrigues-Filho LFS, Ferreira YS, Carneiro J, Asp NE, Shaw PW, Haimovici M, Markaida U, Ready J, Schneider H, Sampaio I (2017) Divergence of cryptic species of Doryteuthis plei Blainville, 1823 (Loliginidae, Cephalopoda) in the Western Atlantic Ocean is associated with the formation of the Caribbean Sea. Mol Phylogenet Evol 106:44–54
Sánchez G, Perry HM, Trigg CB, Vecchione M, Roper CFE, Biesiot RM (1996) Morphometry of juvenile and subadult Loligo pealei and L. plei from the northern Gulf of Mexico. Fish Bull 94:535–550
Sequencher® (2013) Sequence analysis software. Gene Codes Corporation, Ann Arbor, MI, USA. Version 5.2.
Shaw PW, Pierce GJ, Boyle PR (1999) Subtle population structuring within a highly vagile marine invertebrate, the veined squid Loligo forbesi, demonstrated with microsatellite DNA markers. Mol Ecol 8:407–417
Shoemaker JS, Fitch WM (1989) Evidence for molecular sequences that invariable sites should be considered when sequence divergence is calculated. Mol Biol Evol 6(3):270–289
Stat Soft, Inc. (2004) STATISTICA (data analysis software system). Version 7. www.statsoft.com
Schwarz G (1978) Estimating the dimension of a model. Ann Stat 6(2):461–464
Tamura K (1992) Estimation of the number of nucleotide substitutions when there are strong transition-transversion and G+C content biases. Mol Biol Evol 9(4):678–687
Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739
Thompson JD, Higgins DG, 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 Res 22:4673–4380
Vecchione M, Shea E, Bussarawit S, Anderson F, Alexeyev D, Lu C-C, Okutani T, Roeleveld M, Chotiyaputta C, Roper C, Jorgensen E, Sukramongkol N (2005) Systematics of Indo-West Pacific loliginids. Phuket Mar Biol Cent Res Bull 66:23–26
Voss NA, Sweeney MJ (1988) Systematics and biogeography of cephalopods. Volume II. Smiths Contr Zool:277–599
Yang Z (1994) Maximum likelihood phylogenetic estimation from DNA sequences with variable rates over sites: approximate methods. J Mol Evol 39(3):306–314
Young RE, Harman RF (1988) “Larva,” “paralarva” and “subadult” in cephalopod terminology. Malacologia 29(1): 201–207.
Zaleski T, Perez JAA, Gandara-Martins AL (2012) Morphological and morphometric variability of the squid Lolliguncula brevis (Mollusca: Cephalopoda) in Brazilian waters: evidence for two species in the western atlantic? An Acad Bras Ciênc 84(4):1015–1028
Acknowledgments
We thank Dr. Michael Vecchione for his valuable advice and collaboration in making museum material available for the purposes of this research. We thank Mr. Martin Reynaga, fishing entrepreneur from the Port of Tampico, Tamaulipas, and partner of the company Reymar, S.A. for his support in carrying out this project. We are also grateful to the entire crew of the shrimp fishing vessels: Don Bacho, FIPESCO, and Esperanza XI. MDSI wishes to thank BEIFI-IPN [grant for project number 20140781] and CONACyT [grant number 344289] for their financial support during this study.
Funding
This study was funded by Fondo Mixto Tamaulipas-CONACyT 2012–2014 (grant number 177615) and Secretaría de Investigación y Posgrado, Instituto Politécnico Nacional [grant number SIP-IPN 20131165).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical approval
All applicable international, national, and/or institutional guidelines for the care and use of animals were followed by the authors.
Sampling and field studies
It is not applicable.
Data availability
The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request. The sequences generated were deposited in the GenBank (accession numbers MG582539-MG582587).
Additional information
Communicated by M. Vecchione
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Díaz-Santana-Iturrios, M., Salinas-Zavala, C.A., Granados-Amores, J. et al. Taxonomic considerations of squids of the family Loliginidae (Cephalopoda: Myopsida) supported by morphological, morphometric, and molecular data. Mar Biodiv 49, 2401–2409 (2019). https://doi.org/10.1007/s12526-019-00979-3
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12526-019-00979-3