Aggregata polibraxiona n. sp. (Apicomplexa: Aggregatidae) from Octopus bimaculatus Verrill, 1883 (Mollusca: Cephalopoda) from the Gulf of California, Mexico

https://doi.org/10.1016/j.ejop.2021.125825Get rights and content

Highlights

  • Aggregata polibraxiona n. sp. first Apicomplexa described from a cephalopod in Mexico.

  • A. polibraxiona n. sp. is the first Apicomplexa described from Octopus bimaculatus.

  • Morphological description shows cylindrical projections on the sporocyst wall.

  • Molecular characterization shows A. polibraxiona n. sp. close to A. octopiana.

Abstract

The Apicomplexa Aggregata spp. are intracellular parasites of cephalopods that infect the intestinal tract of commercially important species such as Octopus bimaculatus, which sustains the octopus fishery in Baja California (B.C.), Mexico. In this study, Aggregata polibraxiona n. sp. was described from the cecum of O. bimaculatus collected from Bahia de Los Angeles, B. C. Light and electron microscopy revealed that oocysts and sporocysts were spherical to ovoid in shape. Sporulated oocysts (293–835 × 177–688 μm) contained 135–674 sporocysts (12–24 × 11–22 μm). The sporocyst wall was covered by tubular projections (0.55–2.19 μm in length) bifurcated in the top, unevenly distributed, covered by a thin membrane. Each sporocyst contains 11–13 sporozoites (16–26 × 1.20–3 μm). Three partial sequences of the 18S rDNA gene were obtained, and two phylogenetic approaches were performed according to Bayesian inference and Maximum Likelihood. In both phylogenetic reconstructions, the sequences of A. polibraxiona n. sp. were recovered as a monophyletic group within the genus Aggregata and placed as a sister group to Aggregata octopiana Lineage II. Aggregata polibraxiona n. sp. is the first Apicomplexa described from a cephalopod host from Mexico and extends the geographical range of Apicomplexa infecting cephalopods.

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)

  • Z. Yang

    Among-site rate variation and its impact on phylogenetic analyses

    Trends Ecol. Evol.

    (1996)
  • R.F. Ambrose

    Observations on the embryonic development and early post-embryonic behavior of Octopus bimaculatus (Mollusca: Cephalopoda)

    Veliger

    (1981)
  • R.F. Ambrose

    Shelter utilization by the molluscan cephalopod, Octopus bimaculatus

    Mar. Ecol. Prog. Ser.

    (1982)
  • R.F. Ambrose

    Population dynamics of Octopus bimaculatus: influence of life history patterns, synchronous reproduction and recruitment

    Malacologia

    (1988)
  • M.B. Betancor et al.

    Infestación por Aggregata octopiana en pulpo (Octopus vulgaris) durante su engorde en las Islas Canarias

    Rev. Canar. Cienc. Vet.

    (2010)
  • B.P. Berto et al.

    Studies on coccidian oocysts (Apicomplexa: Eucoccidiorida)

    Rev. Bras. Parasitol. Vet.

    (2014)
  • Bush, A.O., Lafferty K.D., Lotz J.M., Shostak, A.W., 1997. Parasitology meets ecology on its own terms: Margolis et al....
  • S. Castellanos-Martínez et al.

    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

    (2014)
  • S. Castellanos-Martínez et al.
  • J. Castresana

    Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis

    Mol. Biol. Evol.

    (2000)
  • Y. Cruz-Quintana et al.

    Pathogens and related diseases in non-European cephalopods: Central and South America

  • C.F.A. Culling et al.

    Cellular Pathology Technique

    (1985)
  • Darriba, D., Taboada, G.L., Doallo, R., Posada, D., 2012. jModelTest 2: more models, new heuristics and parallel...
  • DOF, 2017. Acuerdo por el que se modifica el similar por el que se establece la veda temporal y tallas mínimas de...
  • J.F. Domínguez-Contreras et al.

    Life histories predict genetic diversity and population structure within three species of octopus targeted by small-scale fisheries in Northwest Mexico

    PeerJ

    (2018)
  • J. Estévez et al.

    Aggregata octopiana (Apicomplexa: Aggregatidae) from Octopus vulgaris off NW Spain

    Dis. Aquat. Org.

    (1996)
  • J. Felsenstein

    Confidence limits on phylogenies: and approach using the bootstrap

    Evolution

    (1985)
  • C. Gestal et al.

    Observations on associated histopathology with Aggregata octopiana infection (Protista: Apicomplexa) in Octopus vulgaris

    Dis. Aquat. Org.

    (2002)
  • C. Gestal et al.

    Aggregata octopiana (Protista: Apicomplexa): a dangerous pathogen during commercial Octopus vulgaris ongrowing

    ICES J. Mar. Sci.

    (2007)
  • C. Gestal et al.

    Malabsorption syndrome observed in the common octopus Octopus vulgaris infected with Aggregata octopiana (Protista: Apicomplexa)

    Dis. Aquat. Org.

    (2002)
  • C. Gestal et al.

    Aggregata bathytherma sp. nov. (Apicomplexa: Aggregatidae), a new coccidian parasite associated with a deep-sea hydrothermal vent octopus

    Dis. Aquat. Org.

    (2010)
  • Cited by (7)

    View all citing articles on Scopus
    View full text