Abstract
Immature trematodes of Lecithochirium sp. are recorded for the first time as parasites of the California two-spot octopus Octopus bimaculatus from Bahía de los Ángeles, Baja California, Mexico. Thirty-nine O. bimaculatus were examined for trematodes and a total of 100 immature specimens of Lecithochirium sp. were recorded from the crop of seven infected octopuses. Based on these records, O. bimaculatus may act as a second intermediate or paratenic host for these parasites. Partial sequences of the 28S (region D1-D3) ribosomal gene corroborate the identifications based on morphological characters. DNA sequences of the 28S gene from GenBank were analyzed to include the immature samples of Lecithochirium sp. within a hemiurid phylogenetic framework. All immature specimens of Lecithochirium sp. were recovered as monophyletic and Pulmovermis cyanovitellosus was identified as the sister species of Lecithochirium sp. However, due to the lack of molecular data for species of the genus Lecithochirium, these phylogenetic inferences must be taken with caution. Therefore, the morphological and molecular data obtained here provide a foundation for future work to develop a systematic comparison among- and within-species of the genus Lecithochirium. Additionally, the present records of Lecithochirium in O. bimaculus add to the knowledge of the parasite fauna of cephalopods.
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References
Abdel-Ghaffar F, Abdel-Gaber R, Abdel-Rahman B, Morsy K, Al Quraishy S, Saleh R, Mehlhorn H (2015) Molecular characterization and new geographical record of Lecithochirium priacanthi (Digenea: Hemiuridae) infecting the moontail bullseye fish Priacanthus hamrur (Perciformes: Priacanthidae) from the Red Sea. Egypt Parasitol Res 114:4471–4477. https://doi.org/10.1007/s00436-015-4690-x
Aguirre-Macedo ML, May-Tec AL, Martínez-Aquino A, Cremonte F, Martorelli SR (2017) Diversity of helminth parasites in aquatic invertebrate hosts in Latin America: how much do we know? J Helminthol 91:137–149. https://doi.org/10.1017/S0022149X16000547
Ambrose RF (1984) Food preferences, prey availability, and the diet of Octopus bimaculatus Verrill. J Exp Mar Biol 77:29–44. https://doi.org/10.1016/0022-0981(84)90049-2
Argáez-García N, Guillén-Hernández S, Aguirre-Macedo ML (2010) Intestinal helminths of Lutjanus griseus (Perciformes: Lutjanidae) from three environments in Yucatán (Mexico), with a checklist of its parasites in the Gulf of Mexico and Caribbean region. Rev Mex Biodiv 81:903–912
Armendáriz-Villegas EJ, Ceballos-Vázquez BP, Markaida U, Abitia-Cárdenas A, Medina-López MA, Arellano-Martínez M (2014) Diet of Octopus bimaculatus Verril, 1883 (Cephalopoda: Octopodidae) in Bahía de los Ángeles, Gulf of California. J Shellfish Research 33:305–314. https://doi.org/10.2983/035.033.0129
Atopkin DM, Besprozvannykh VV, Beloded AY, Ngoc HD, Ha NV, Tang NV (2017) Phylogenetic relationships of Hemiuridae (Digenea: Hemiuroidea) with new morphometric and molecular data of Aphanurus mugilis Tang, 1981 (Aphanurinae) from mullet fish of Vietnam. Parasitol Inter 66:824–830. https://doi.org/10.1016/j.parint.2017.09.009
Atopkin D, Nakao M, Besprozvannykh V, Ha N, Nguyen H, Sasaki M (2020) Morphological and molecular data for species of Lecithaster Lühe, 1901 and Hysterolecithoides Yamaguti, 1934 (Digenea: Lecithasteridae) from fish of East Asia and phylogenetic relationships within the Hemiuroidea Looss, 1899. J Helminthol 94:E14. https://doi.org/10.1017/S0022149X18001049
Bao M, Roura A, Mota M, Nachón DJ, Antunes C, Cobo F, MacKenzie K, Pascual S (2015) Macroparasites of allis shad (Alosa alosa) and twaite shad (Alosa fallax) of the Western Iberian Peninsula Rivers: ecological, phylogenetic and zoonotic insights. Parasitol Res 114:3721–3739. https://doi.org/10.1007/s00436-015-4601-1
Bartoli P, Gibson DI (2007) The status of Lecithochirium grandiporum (Rudolphi, 1819) (Digenea: Hemiuridae), a rarely reported and poorly known species from the Mediterranean moray eel Muraena helena L. in the Western Mediterranean. Syst Parasitol 68:183–194. https://doi.org/10.1007/s11230-007-9095-5
Blasco-Costa I, Poulin R (2017) Parasite life-cycle studies: a plea to resurrect an old parasitological tradition. J Helminthol 91:647–656. https://doi.org/10.1017/S0022149X16000924
Bray RA (1991) Hemiuridae (Digenea) from marine fishes of the southern Indian Ocean: Genus Lecithochirium Lühe, 1901 (Lecithochiriinae). Syst Parasitol 18:193–219. https://doi.org/10.1007/BF00009360
Bush AO, Lafferty KD, Lotz JM, Shostak AW (1997) Parasitology meets ecology on its own terms; Margolis et al. revisited. J Parasitol 83:575–583. https://doi.org/10.2307/3284227
Calhoun DM, Curran SS, Pulis EE, Provaznik JM, Franks JM (2013) Hirudinella ventricosa (Pallas, 1774) Baird, 1853 represents a species complex based on ribosomal DNA. Syst Parasitol 86:197–208. https://doi.org/10.1007/s11230-013-9439-2
Castresana J (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 17:540–555. https://doi.org/10.1093/oxfordjournals.molbev.a026334
Centeno-Chalé OA, Aguirre-Macedo ML, Gold-Bouchot G, Vidal-Martínez VM (2015) Potential effects of chemical pollution on the helminth communities of the Mexican flounder Cyclopsetta chittendeni from the Campeche sound, Gulf of Mexico. Ecotoxicol Environ Safety 119:162–169. https://doi.org/10.1016/j.ecoenv.2015.04.030
Claxton AT, Fuehring AD, Andres MJ, Moncrief TD, Curran SS (2017) Parasites of the vermilion snapper, Rhomboplites aurorubens (Cuvier), from the Western Atlantic Ocean. Comp Parasitol 84:1–14. https://doi.org/10.1654/1525-2647-84.1.1
Colunga-Ramírez GE, Martínez-Aquino A, Flores-López CA, Gestal C, Azevedo C, Castellanos-Martíne S (2021) Aggregata polibraxiona n sp (Apicomplexa: Aggregatidae) from Octopus bimaculatus Verrill, 1883 (Mollusca: Cephalopoda) from the Gulf of California. Mexico. Europ J Protistol 81:125825
Darriba D, Taboada G, Doallo R, Posada (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9:772. https://doi.org/10.1038/nmeth.2109
Drummond AJ, Ashton B, Buxton S, Cheung M, Cooper A, Heled J, Kearse M, Moir R, Stones-Havas S, Sturrock S, Thierer T, Wilson A (2010) Geneious v5.1, Available at http://www.geneious.com (Accessed 15/03/2022)
Estrada-García MA, García-Prieto L, Garrido-Olvera L (2018) Description of a new species of Pseudopecoelus (Trematoda: Opecoelidae) with new records of trematodes of marine fishes from the Pacific coast of Mexico. Rev Mex Biodiv 89:22–28
García-Teh JG, Vidal-Martínez VM, Mariño-Tapia I, Árcega-Cabrera F, Ordoñez-López U, Aguirre-Macedo ML (2021) Metazoan parasite infracommunities of the Tomtate Grunt (Haemulon aurolineatum) as potential bioindicators of environmental conditions in the Yucatan Continental Shelf, Mexico. Bull Environ Contam Toxicol 108:49–54. https://doi.org/10.1007/s00128-021-03305-5
Gestal C, Pascual S, Guerra Á, Fiorito G, Vieites J (2019) Handbook of pathogens and diseases in cephalopods. Springer, Cham. https://doi.org/10.1007/978-3-030-11330-8
Gibson DI (2002) Family Hemiuridae Looss, 1899. In Gibson DI, Jones A, Bray RA (eds), Keys to the Trematoda, Vol. 1. Wallingford: CAB International, pp. 305–340
Gibson DI, Bray RA (1979) The Hemiuroidea: terminology, systematics and evolution. Bull Br Mus Nat Hist (zool) 36:35–146
Gibson DI, Bray RA (1986) The Hemiuridae (Digenea) of fishes from the north-east Atlantic. Bull Br Mus Nat Hist (zool) 51:1–125
Guillén-Hernández S, López-Struck A, González-Salas C, Aguirre-Macedo ML (2018) Octopus maya parasites of the Yucatán Península, Mexico. I Faunal Assemblages Dis Aquat Org 130:37–43. https://doi.org/10.3354/dao03249
Hochberg FG (1990) Diseases of Mollusca: Cephalopoda (Diseases caused by protistans and metazoans). In: Kinne O (ed) Diseases of Marine Animals. Biologische Anstalt Helgoland, Germany, pp 47–200
Katoh K, Standley DM (2016) A simple method to control over-alignment in the MAFFT multiple sequence alignment program. Bioinform 32:1933–1942. https://doi.org/10.1093/bioinformatics/btw108
Krupenko D, Gonchar A, Kremnev G, Uryadova A (2020) On the life cycle of Hemiurus levinseni Odhner, 1905 (Digenea: Hemiuridae). Invertebrate Zoology 17:205–218. https://doi.org/10.15298/invertzool.17.3.01
Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35:1547–1549. https://doi.org/10.1093/molbev/msy096
López-Peraza DJ, Hernández-Rodríguez M, Barón-Sevilla B (2018) Fatty acid profile, proteolytic activity and survival of Octopus bimaculatus paralarvae fed with enriched Artemia franciscana. Molluscan Res 38:227–237. https://doi.org/10.1080/13235818.2018.1428485
López-Peraza DJ, Hernández-Rodríguez M, Barón-Sevilla B, Bückle-Ramírez LF, Grano-Maldonado MI (2017) First record of Stibarobdella moorei (Annelida, Hirudinea, Piscicolidae) a marine leech parasitizing Octopus bimaculatus (Mollusca: Octopodidae) from the Mexican Pacific coast. Helminthologia 54:322–329. https://doi.org/10.1515/helm-2017-0044
Madhavi R, Bray RA (2018) Superfamily Hemiuroidea Looss, 1899. In: Madhavi R, Bray RA (Eds) Digenetic Trematodes of Indian Marine Fishes. Crown, 119–262. https://doi.org/10.1007/978-94-024-1535-3_17
Martínez-Aquino A, Vidal-Martínez VM, Aguirre-Macedo ML (2017) A molecular phylogenetic appraisal of the acanthostomines Acanthostomum and Timoniella and their position within Cryptogonimidae (Trematoda: Opisthorchioidea). PeerJ 5:e4158. https://doi.org/10.7717/peerj.4158
Martínez-Aquino A, Vidal-Martínez VM, Ceccarelli FS, Méndez O, Soler-Jiménez LC, Aguirre-Macedo ML (2020) Phylogeny, genetics, and the partial life cycle of Oncomegas wageneri in the Gulf of Mexico. Current Zoology 66:275–283. https://doi.org/10.1093/cz/zoz045
McConnaughey BH (1949) Mesozoa of the family Dicyemidae from California. Univ Calif Publ Zool 55:1–34
Mendoza-Cruz M, Valles-Vega I, Lozano-Cobo H, Gómez del Prado RMC, Castro-Moreno PN (2013) Parasite fauna of Paranthias colonus (Valenciennes, 1846) from El Sargento, Baja California Sur, Mexico. Neotrop Helminthol 7:13–28
Miller MA, Pfeiffer W, Schwartz T (2010) Creating the CIPRES Science Gateway for inference of large phylogenetic trees. Proceedings of the Gateway Computing Environments Workshop (GCE), 14 November 2010. New Orleans (LA): IEEE Computer Society 1–8.
Monroy-Escamilla, M (2005) Estudio taxonómico de algunos tremátodos parásitos de peces del Golfo de California. B. S. Thesis (In Spanish), Facultad de Ciencias, Universidad Nacional Autónoma de México, Mexico City, pp 68.
Montoya-Mendoza J, Jiménez-Badillo L, Salgado-Maldonado G, Mendoza-Franco EF (2014) Helminth parasites of the red snapper, Lutjanus campechanus (Perciformes: Lutjanidae) from the Reef Santiaguillo, Veracruz, Mexico. J Parasitol 100:868–872. https://doi.org/10.1645/13-429.1
Nadler SA, Hudspeth DSS (1998) Ribosomal DNA and phylogeny of the Ascaridoidea (Nematoda: Secernentea): implications for morphological evolution and classification. Mol Phylogenet Evol 10:221–236. https://doi.org/10.1006/mpev.1998.0514
Olson PD, Cribb TH, Tkach VV, Bray RA, Littlewood DTJ (2003) Phylogeny and classification of the Digenea (Platyhelminthes: Trematoda). Int J Parasitol 33:733–755. https://doi.org/10.1016/S0020-7519(03)00049-3
Overstreet RM, Hochberg FG (1975) Digenetic trematodes in cephalopods. J Mar Biol Assoc UK 55:893–910. https://doi.org/10.1017/S0025315400017781
Pankov P, Webster BL, Blasco-Costa I, Gibson DI, Littlewood DTJ, Balbuena JA, Kostadinova A (2006) Robinia aurata n. g., n. sp. (Digenea: Hemiuridae) from the mugilid Liza aurata with a molecular confirmation of its position within the Hemiuroidea. Parasitol 133:217–227. https://doi.org/10.1017/S0031182006000126
Pascual S, Abollo E, Mladineo I, Gestal C (2019) Metazoa and related diseases. In: Gestal C, Pascual S, Guerra Á, Fiorito G and Vieites J (Eds). Handbook of Pathogens and Diseases in Cephalopods. Springer, Cham, pp 169–179. https://doi.org/10.1007/978-3-030-11330-8_12
Pérez-Ponce de León G, García-Prieto L, Mendoza-Garfias B (2007) Trematode parasites (Platyhelminthes) of wildlife vertebrates in Mexico. Zootaxa 1534:1–247
Posada D (2003) Using MODELTEST and PAUP* to select a model of nucleotide substitution. In: Baxevanis AD, Davison DB, Page RDM, Petsko GA, Stein LD, Stormo GD (Eds) Current Protocols in Bioinformatics. John Wiley and Sons, New York, 6.5.1–6.5.14. https://doi.org/10.1002/0471250953.bi0605s00
Rambaut A (2009) FigTree: tree figure drawing tool. University of Edinburgh, Edinburgh, Institute of Evolutionary Biology. http://tree.bio.ed.ac.uk/software/figtree/
Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542. https://doi.org/10.1093/sysbio/sys029
Saiki RK, Gelfand DH, Stoffel S, Scharf SJ, Higuchi R, Horn GT, Mullis KB, Erlich HA (1988) Primer-directed enzymatic amplification of DNA with a thermostable DNA polymerase. Science 239:487–491. https://doi.org/10.1126/science.2448875
Schwarz G (1978) Estimating the dimension of a model. Ann Stat 6:461–464. https://doi.org/10.1214/aos/1176344136
Sokolov SG, Atopkin DM, Urabe M, Gordeev II (2019) Phylogenetic analysis of the superfamily Hemiuroidea (Platyhelminthes, Neodermata: Trematoda) based on partial 28S rDNA sequences. Parasitol 146:596–603. https://doi.org/10.1017/S0031182018001841
Stecher G, Tamura K, Kumar S (2020) Molecular evolutionary genetics analysis (MEGA) for macOS. MBE 37:1237–1239. https://doi.org/10.1093/molbev/msz312
Stock SP, Campbell JF, Nadler SA (2001) Phylogeny of Steinernema travassos, 1927 (Cephalobina: Steinernematidae) inferred from ribosomal DNA sequences and morphological characters. J Parasitol 87:877–889. https://doi.org/10.1645/0022-3395(2001)087[0877:POSTCS]2.0.CO;2
Talavera G, Castresana J (2007) Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Syst Biol 56:564–577. https://doi.org/10.1080/10635150701472164
Vidal-Martínez VM, Aguirre-Macedo ML, Scholz T, González-Solís D, Mendoza-Franco E (2001) Atlas of the helminth parasites of cichlid fishes of Mexico. Academia, Praha, p 166
Vidal-Martínez VM, Centeno-Chalé OA, Torres-Irineo E, Sánchez-Ávila JI, Gold-Bouchot G, Aguirre-Macedo ML (2014) The metazoan parasite communities of the shoal flounder (Syacium gunteri) as bioindicators of chemical contamination in the southern Gulf of Mexico. Parasites Vectors 7:541. https://doi.org/10.1186/s13071-014-0541-3
Vidal-Martínez VM, Velázquez-Abunader I, Centeno-Chalé OA, May-Tec AL, Soler-Jiménez C et al (2019) Metazoan parasite infracommunities of the dusky flounder (Syacium papillosum) as bioindicators of environmental conditions in the continental shelf of the Yucatan Peninsula. Mexico Parasite Vectors 12:277. https://doi.org/10.1186/s13071-019-3524-6
Wiens JJ, Moen DS (2008) Missing data and the accuracy of Bayesian phylogenetics. J Syst Evol 43:307–314
WoRMS (2022) Lecithochirium Lühe 1901. http://www.marinespecies.org/aphia.php?p=taxdetails&id=108758 (2022–03–15)
Yamaguti, S. (1970). Digenetic trematodes of Hawaiian fishes. Tokyo, Keigaku, pp 436.
Acknowledgements
We are grateful to Arturo Rincón Sandoval (Ms. Sc. student, Maestría y Doctorado en Ciencias e Ingeniería [MyDCI], Facultad de Ciencias, Universidad Autónoma de Baja California [UABC], Mexico) for technical support with the microscopy equipment. We are grateful to Abril Gamboa and David Hernández-Mena for technical assistance in the molecular lab (CINVESTAV-IPN, Merida, Yucatán, Mexico). Thanks to Graciela E. Colunga-Ramírez, Jesus Galarza, and Jorge Sánchez-Solís for their help during fieldwork. AJCM was supported by a CONACyT scholarship (No. 712235) to accomplish his Ms. Sc. degree. We also thank Dr. Fadia Sara Ceccarelli of the Center for Scientific Research and Higher Education at Ensenada, Mexico (CICESE) who reviewed the first draft of this manuscript and made very useful suggestions of the phylogenetic analyses that we present in this contribution. We are grateful to Sean M. Rovito for help with the language editing and for his constructive criticism. The manuscript greatly benefited from comments of two anonymous referees.
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This work was financially supported from Grant No. 286347 by the Consejo Nacional de Ciencia y Tecnología (CONACyT) to SCM, partially funded by the Grant No. 201441 (CONACyT, Mexican Ministry of Energy, Hydrocarbon Trust) to MLAM, and also partially funded by the Grant No. 400/2356 (Programa para el Desarrollo Profesional Docente [UABC–PRODEP–2019] from Secretaría de Educación Pública [SEP], Mexico) to AMA.
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AJCM collected samples in the laboratory, mounted and made the preliminarily identification of the specimens, produced the molecular data, carried out the formal analysis, and prepared the figures and tables. SCM conceived the study, made the field observations, acquired funding and contributed reagents/materials/analysis tools. MLAM contributed reagents/materials/analysis tools, identified the specimens, and acquired funding. AMA conceived the research, acquired funding, identified the specimens, prepared figures and tables, and carried out the formal analysis, data curation, visualization, writing—original draft, writing—review and editing. All authors reviewed the manuscript.
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Chan-Martin, A.d., Castellanos-Martínez, S., Aguirre-Macedo, M.L. et al. Immature trematodes of Lecithochirium sp. (Digenea: Hemiuridae) in the California two-spot octopus (Octopus bimaculatus) from Mexico. Parasitol Res 121, 2651–2660 (2022). https://doi.org/10.1007/s00436-022-07590-9
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DOI: https://doi.org/10.1007/s00436-022-07590-9