Aggregata polibraxiona n. sp. (Apicomplexa: Aggregatidae) from Octopus bimaculatus Verrill, 1883 (Mollusca: Cephalopoda) from the Gulf of California, Mexico
Graphical abstract
Introduction
Apicomplexa Aggregata Frenzel, 1885 (Apicomplexa: Aggregatidae) are parasites that infect the intestinal tract of their definitive wild and reared cephalopod host (Berto et al., 2014, Hochberg, 1990). Aggregata spp. are heteroxenous endoparasites that require two hosts to complete their life cycle, a crustacean and a cephalopod species as intermediate and definitive hosts, respectively. The asexual (merogonial) stages develop within the gut of crustaceans, while the sexual (gamogonial and sporogonial) stages develop within the intestinal tract of the definitive cephalopod host (Gestal et al., 2002a, Hochberg, 1990).
Aggregata spp. are found within the mucous membrane’s epithelial cells and submucosal connective tissue of the cecum and gut. The parasite causes severe histopathological and functional damage to the cephalopod gastrointestinal tract. Histopathological lesions include pericyst reactions of connective tissue, hemocytic infiltration, and distention of the tissue infected, while functional damage includes malabsorption syndrome (Castellanos-Martínez et al., 2019, Cruz-Quintana et al., 2019, Gestal et al., 2002b, Gestal et al., 2002c).
Ten species of the genus Aggregata have been described worldwide (Castellanos-Martínez et al., 2013, Supplementary Table S1) based on morphological characters of the sporogonial stages (i.e., size and the ultrastructural sporocyst wall) and the number of sporozoites inside the sporocysts (Gestal et al., 2010, Hochberg, 1990). The use of these morphological characters combined with molecular markers and ecological data have been used to improve the characterization and phylogenetic relationships of Aggregata species to enhance our understanding of their evolutionary history (Castellanos-Martínez et al., 2013, Mathur et al., 2021, Tedesco et al., 2017). The small subunit 18S ribosomal RNA gene (18S rDNA) has been utilized for molecular characterization and phylogenetic relationships of Aggregatidae (Castellanos-Martínez et al., 2013, Kopečná et al., 2006, Kristmundsson and Freeman, 2018, Tedesco et al., 2017). However, only two species of cephalopod parasites have DNA sequences available to date (Castellanos-Martínez et al., 2013, Kopečná et al., 2006, Tedesco et al., 2017), i.e. Aggregata octopiana (Schneider, 1875), which infects the common octopus, Octopus vulgaris Cuvier, 1797; and Aggregata eberthi Labbé, 1895, that infects the common cuttlefish, Sepia officinalis Linnaeus, 1758.
In the North East (NE) Pacific Ocean three species of Aggregata have been described: Aggregata millerorum Poynton, Reimschuessel and Stoskopf, 1992 from Octopus bimaculoides Pickford and McConnaughey, 1949; Aggregata dobelli Poynton, Reimschuessel and Stoskopf, 1992 from Enteroctopus dofleini (Wülker, 1910); and Aggregata bathytherma Gestal, Pascual and Hochberg, 2010 from Vulcanoctopus hydrothermalis González et al., 1998. In Mexico, gross observations and histopathological lesions caused by the infection of Aggregata sp. have been recorded in Octopus maya Voss and Solís, 1966 from Yucatán (Cruz-Quintana et al., 2019, Guillén-Hernández et al., 2018). Occasional records of Aggregata sp. infection are known from cephalopods from the Mexican Pacific. However, a formal description of Apicomplexa of the genus Aggregata spp. infecting a cephalopod host from Mexico is lacking (Hochberg, 1990).
Octopus bimaculatus Verrill, 1883 has a continuous geographical distribution that extends from Southern California to the Gulf of California (Ambrose, 1982, Domínguez-Contreras et al., 2018, Jereb et al., 2014). It is the target octopus species in Bahia de Los Angeles, which is the most economically important locality for the octopus fishery in Baja California (B. C.) (Domínguez-Contreras et al., 2018, López-Rocha et al., 2012). To date, studies performed on O. bimaculatus have focused on embryonic development (Ambrose, 1981), feeding habits (Ambrose, 1984, Villegas et al., 2014), population dynamics (Ambrose, 1988), growth (López-Rocha et al., 2012), distribution (Domínguez-Contreras et al., 2018) and the fatty acids composition of hatched paralarvae (López-Peraza et al., 2018). Contrarily, the only symbionts reported in O. bimaculatus are the dicyemid Dicyemennea abelis (McConnaughey, 1949) and the marine leech, Stibarobdella moorei (López-Peraza et al., 2017).
Octopus bimaculatus is a candidate species to develop octopus aquaculture in the Mexican Northwest (López-Peraza et al., 2017, López-Peraza et al., 2018). It is well known that culture conditions favor parasite transmission, exacerbate pathologies, and might promote diseases caused by potential pathogens, or even apparently harmless symbionts in wild populations (Roumbedakis et al., 2018). Thus, the first step to face a disease outbreak is to know the etiological agent. Hence, the present study aimed to describe the Apicomplexa, Aggregata polibraxiona n. sp., infecting O. bimaculatus from Bahia de Los Angeles, B.C., Mexico.
Section snippets
Sample collection
Fresh O. bimaculatus (n = 34) were collected by traps in Bahia de Los Angeles (29°00′′N, 113°30′′W) in April and May 2018; and January 2019 (Table 1) from the commercial artisanal fishery that takes place from August 1st to November 30th of every year in the locality (DOF, 2017). The specimens were transported on ice to the Instituto de Investigaciones Oceanológicas, at the Universidad Autónoma de Baja California, Mexico and immediately processed when arrived at the laboratory. The following
Results
From 34 O. bimaculatus analyzed, 32% were females and 68% males (Table 1). The prevalence and mean intensity of infection were 100% and 1.92 × 106 ± 2.07 × 106 S/G, respectively. Developmental parasitic stages (i.e., gamogony and sporogony) were found in the cecum submucosa causing loss of epithelial cells, tissue distension, and hemocytic infiltration (Fig. 3). Morphological and molecular analyses indicate that the apicomplexan infecting O. bimaculatus in Bahia de Los Angeles corresponds to a
Discussion
This work describes the first Aggregata species in a cephalopod host from Mexico based on morphological and molecular data. Aggregata polibraxiona n. sp. from O. bimaculatus, is the fourth species described from the NE Pacific Ocean, the other three being A. millerorum from O. bimaculoides, A. dobelli from E. dofleini and A. bathytherma from V. hydrothermalis (Gestal et al., 2010, Poynton et al., 1992). According to the diagnosis of the genus given by Gestal et al., 2010, Poynton et al., 1992,
CRediT authorship contribution statement
Graciela Esmeralda Colunga-Ramírez: Investigation, Formal analysis, Data curation, Visualization, Writing -original draft, Writing - review & editing. Andrés Martínez-Aquino: Formal analysis, Data curation, Visualization, Writing -original draft, Writing - review & editing. Carlos Alberto Flores-López: Resources, Formal analysis, Writing - review & editing. Camino Gestal: Resources, Formal analysis, Investigation, Writing - review & editing. Carlos Azevedo: Resources, Formal analysis,
Declaration of Competing Interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgments
This work was supported by the National Council on Science and Technology, Mexico (CONACYT, Mexico; project number: 286347). G.E.C.R. was supported by CONACyT, Mexico (grant number: 769732/632044). We are grateful to Ana Ruth Cristobal, Patricia Quintana Owen (National Laboratory for the Study of Nano- and Biomaterials, CINVESTAV-IPN, Merida, Yucatán, Mexico) and Jesús Méndez (Centre for Scientific and Technological Support to Research, University of Vigo, Spain) for their technical support
References (63)
Food preferences, prey availability, and the diet of Octopus bimaculatus Verrill
J. Exp. Mar. Biol.
(1984)- et al.
Proteomic characterization of the hemolymph of Octopus vulgaris infected by the protozoan parasite Aggregata octopiana
J. Proteomics
(2014) - et al.
Molecular phylogenetic analysis of the coccidian cephalopod parasites Aggregata octopiana and Aggregata eberthi (Apicomplexa: Aggregatidae) from the NE Atlantic coast using 18S rRNA sequences
Eur. J. Protistol.
(2013) Refinement of pepsin digestion method for isolation of Toxoplasma gondii from infected tissues
Vet. Parasitol.
(1998)- et al.
On the life cycle of Aggregata eberthi and observations on Aggregata octopiana (Apicomplexa, Aggregatidae) from Galicia (NE Atlantic)
Europ. J. Protistol.
(2002) - et al.
Phylogenetic analysis of coccidian parasites from invertebrates: search for missing links
Protist
(2006) - et al.
Aggregata (Protozoa: Apicomplexa) infection in the common octopus Octopus vulgaris from the West Mediterranean Sea: the infection rates and possible effect of faunistic, environmental and ecological factors
J. Sea Res.
(2013) - et al.
Multiple independent origins of apicomplexan-like parasites
Curr. Biol.
(2019) - et al.
First ultrastructural and molecular phylogenetic evidence from the Blastogregarines, an early branching lineage of plesiomorphic Apicomplexa
Protist
(2018) - et al.
Morphological and molecular characterization of Aggregata spp. Frenzel, 1885 (Apicomplexa: Aggregatidae) in Octopus vulgaris Cuvier, 1797 (Mollusca: Cephalopoda) from Central Mediterranean
Protist
(2017)
Among-site rate variation and its impact on phylogenetic analyses
Trends Ecol. Evol.
Observations on the embryonic development and early post-embryonic behavior of Octopus bimaculatus (Mollusca: Cephalopoda)
Veliger
Shelter utilization by the molluscan cephalopod, Octopus bimaculatus
Mar. Ecol. Prog. Ser.
Population dynamics of Octopus bimaculatus: influence of life history patterns, synchronous reproduction and recruitment
Malacologia
Infestación por Aggregata octopiana en pulpo (Octopus vulgaris) durante su engorde en las Islas Canarias
Rev. Canar. Cienc. Vet.
Studies on coccidian oocysts (Apicomplexa: Eucoccidiorida)
Rev. Bras. Parasitol. Vet.
De novo transcriptome sequencing of the Octopus vulgaris hemocytes using Illumina RNA-Seq technology: response to the infection by the gastrointestinal parasite Aggregata octopiana
PLoS ONE
Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis
Mol. Biol. Evol.
Pathogens and related diseases in non-European cephalopods: Central and South America
Cellular Pathology Technique
Life histories predict genetic diversity and population structure within three species of octopus targeted by small-scale fisheries in Northwest Mexico
PeerJ
Aggregata octopiana (Apicomplexa: Aggregatidae) from Octopus vulgaris off NW Spain
Dis. Aquat. Org.
Confidence limits on phylogenies: and approach using the bootstrap
Evolution
Observations on associated histopathology with Aggregata octopiana infection (Protista: Apicomplexa) in Octopus vulgaris
Dis. Aquat. Org.
Aggregata octopiana (Protista: Apicomplexa): a dangerous pathogen during commercial Octopus vulgaris ongrowing
ICES J. Mar. Sci.
Malabsorption syndrome observed in the common octopus Octopus vulgaris infected with Aggregata octopiana (Protista: Apicomplexa)
Dis. Aquat. Org.
Aggregata bathytherma sp. nov. (Apicomplexa: Aggregatidae), a new coccidian parasite associated with a deep-sea hydrothermal vent octopus
Dis. Aquat. Org.
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