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Finding a needle in a haystack: larval stages of Didymozoidae (Trematoda: Digenea) parasitizing marine zooplankton

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Abstract

Larval didymozoids (Trematoda: Digenea) were discovered parasitizing the hemocoel of the heteropod Firoloida desmarestia (redia mean intensity = 13) and the chaetognaths Flaccisagitta enflata and Flaccisagitta hexaptera (metacercaria mean intensity = 1) during a 2014–2016 systematic study of parasites of zooplankton collected in the central and southern regions of the Gulf of California, Mexico. Didymozoid infection route during the early life cycle was inferred combining morphological (light microscopy) and molecular (mitochondrial cytochrome c oxidase subunit I gene, cox1) evidence. Didymozoid rediae parasitizing F. desmarestia were observed, just after field collection of the host, containing hundredths of completely developed cystophorous cercariae, releasing them though the birth pore at approximately one cercaria every 12 s. Cercariae lost their tails developing into a ‘young metacercaria’ in 1 d at 22 °C without need of an intermediate host. Molecular analysis of cox1 showed that rediae found in F. desmarestia belong to two distinct didymozoid species (Didymozoidae sp. 1 and sp. 2). Metacercariae parasitizing chaetognaths were morphologically identified as Didymozoidae type Monilicaecum and cox1 sequences showed that metacercariae of chaetognaths matched with these two Didymozoidae sp. 1, and sp. 2 species found parasitizing F. desmarestia, plus a third distinct Didymozoidae sp. 3. These are the first DNA sequences of cox1 gene from didymozoid larvae for any zooplankton taxonomic group in the world. We concluded that F. desmarestia is the first intermediate host of rediae and cercariae, and the chaetognaths are the second intermediate hosts where non-encysted metacercariae were found. The definitive host is still unknown because cox1 sequences of present study did not genetically match with any available cox1 sequence of adult didymozoid. Our results demonstrate a potential overlap in the distribution of two carnivorous zooplankton taxonomic groups that are intermediate hosts of didymozoids in the pelagic habitat. The didymozoid specimens were not identified to species level because any of the cox1 sequences generated here matched with the sequences of adult didymozoids currently available in GenBank and Bold System databases. This study provides baseline information for the future morphological and molecular understanding of the Didymozoidae larvae that has been previously based on the recognition of the 12 known morphotypes.

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Acknowledgements

We thank Captain Pascual Barajas and the crew of the R/V El Puma and graduate students and researchers of the Fisheries Ecology Laboratory of the Instituto de Ciencias del Mar y Limnología (UNAM, Mexico City) and CICIMAR-IPN for their assistance with the zooplankton sampling. We deeply thank María del Carmen Gómez del Prado-Rosas for the facilities to do technical parasitological work at the Parasitology Laboratory (UABCS, La Paz, BCS, Mexico) and Clarisse Louvard (University of Queensland) by sharing valuable information about her publication Louvard et al. (2022). We deeply thank Dra. Patricia Cortés-Calva and M.Sc. Griselda F. Gallegos-Simental for the technical work extracting, amplifying, and sequencing the trematode specimens at the Nodo del Código de Barras de la Vida, MEXBOL at CIBNOR, La Paz, BCS, Mexico.

Funding

The Instituto Politécnico Nacional, Centro Interdisciplinario de Ciencias Marinas (SIP 2014–2022), Consejo Nacional de Ciencia y Tecnología-Ciencia Básica (2012–178615–C01, 2016–284201-C01) (projects administrator J.G.-G.), and Instituto de Ciencias del Mar y Limnología, Universidad Nacional Autónoma de México (PAPIIT, UNAM grant IN20066610–3 and CONACyT Ciencia Básica 2010–152850–C01, A1-S-21459) (projects administrator C.J.-R.) provided research funds to do the present study. We thank the project MEXBOL Barcode of Life to sequence zooplankton and their parasites in Los Cabos region; Project Code “ZPCR” for financial support the molecular analysis of parasites used in the present study Código de Barras de la Vida MEXBOL (project administrator J.G.-G.), and CONACyT 2018–295569, (project administrator Patricia Cortés-Calva). CONACyT Red Temática Código de barras de la vida de México (2011) also provided funds to the present study. H.L.-C. was supported by a PhD CONACyT (A14618), PIFI-IPN (SIP20110012) and BEIFI-IPN (SIP20140497, 20150113, 20160495, 20171275) doctoral grants. All the authors are SNI fellows, and J.G.-G. is also a COFAA-IPN and EDI-IPN fellow.

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Authors and Affiliations

  1. Departamento de Hidrobiología, Universidad Autónoma Metropolitana, Unidad Iztapalapa, Av. Ferrocarril de San Rafael Atlixco 186, Col. Leyes de Reforma, 09310, Mexico City, Mexico

    Horacio Lozano-Cobo

  2. Departamento de Plancton y Ecología Marina, Centro Interdisciplinario de Ciencias Marinas, Instituto Politécnico Nacional, Av. IPN s/n, 23096, La Paz, B.C.S, Mexico

    Horacio Lozano-Cobo & Jaime Gómez-Gutiérrez

  3. Laboratorio de Helmintología, Departamento de Zoología, Instituto de Biología, Universidad Nacional Autónoma de México, Tercer circuito s/n, Ciudad Universitaria, 04510, Mexico City, Mexico

    Alejandro Oceguera-Figueroa

  4. Departamento Académico de Ingeniería en Pesquerías, Universidad Autónoma de Baja California Sur, km 5.5 Carretera al Sur, 23080, La Paz, B.C.S, Mexico

    Claudia A. Silva-Segundo

  5. Instituto de Ciencias del Mar y Limnología, Universidad Nacional Autónoma de México, Tercer circuito s/n, Ciudad Universitaria, 04510, Mexico City, Mexico

    Carlos J. Robinson

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  1. Horacio Lozano-Cobo
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  5. Jaime Gómez-Gutiérrez
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Contributions

Horacio Lozano Cobo, original idea, sampling and specimen transportation, morphological identification of parasites and hosts, preparation of manuscript and edition of figures, text and videos; Claudia Alicia Silva-Segundo, molecular analysis and text edition; Alejandro Oceguera-Figueroa, molecular analysis and text edition; Carlos Jorge Robinson, sampling and specimens transportation, text edition and project administrator; Jaime Gómez-Gutiérrez, original idea, sampling and specimen transportation, preparation of manuscript and text and figure and video edition, and project administrator.

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Correspondence to Horacio Lozano-Cobo or Jaime Gómez-Gutiérrez.

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The zooplankton sampling and specimen analysis protocols that were developed in the present study fully complied with the ethical principles of animal experimentation prepared by regulations of the Mexican government.

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Lozano-Cobo, H., Oceguera-Figueroa, A., Silva-Segundo, C.A. et al. Finding a needle in a haystack: larval stages of Didymozoidae (Trematoda: Digenea) parasitizing marine zooplankton. Parasitol Res 121, 2661–2672 (2022). https://doi.org/10.1007/s00436-022-07593-6

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