First molecular detection of the parasites Molicola uncinatus and Hepatoxylon trichiuri (Cestoda: Trypanorhyncha) infecting the silver scabbardfish Lepidopus caudatus from the Central Mediterranean Sea: Implications for the seafood quality and safety

Abstract

Trypanorhynch tapeworms are marine heteroxenous parasites, involving sharks and rays as definitive hosts, invertebrates (i.e. crustaceans) as first intermediate hosts, and various teleost fishes as intermediate/paratenic ones. The massive presence of Trypanorhyncha larval forms in the flesh or body cavity of the fish hosts reduces their market value, making them unappealing to consumers, or causing discards of fish products. The identification of merocercoids (N = 100) of Molicola uncinatus and plerocercoids (N = 46) of Hepatoxylon trichiuri parasitizing the silver scabbardfish, Lepidopus caudatus, from the Central Mediterranean Sea (off Malta coast), was obtained, for the first time, by using sequences analysis of the complete small subunit (ssrDNA) and the partial large subunit (lsrDNA) ribosomal RNA gene loci. The Bayesian Inference from the concatenated sequences obtained at the two gene loci showed that the individuals of M. uncinatus and H. trichiuri clustered, respectively, in two well distinct and supported phylogenetic lineages, corresponding to the two cestode species. High prevalence (P) and mean abundance (MA) values were observed in the infection with merocercoids of M. uncinatus (P = 100%, A = 28.81), with the ventral musculature of the silver scabbardfish as the most parasitized site. Plerocercoids of H. trichiuri were found to infect only the mesenteries, attached to various fish tissues, with a mean abundance rate of 1.28. Even if harmless to humans, a heavy parasitic load with larval stages of Trypanorhyncha, particularly in the edible part of the silver scabbardfish (as here reported for merocercoids of M. uncinatus), can compromise the appearance of the fish-food, making it repugnant and unappealing for the final consumer. It has been also discussed that when managing the risk related to parasites affecting the fish quality and safety of fisheries products, the fishing ground where the life cycle of those parasites takes place should be also taken into account, as it would include the ecological drivers of the infection with those parasites. This wider ecological approach would be of help to the Food Business Operators (FBOs), gathering knowledge useful to manage fisheries in a wide "One-Health" perspective, aware of sustainability, quality and consumer safety aspects of seafood production.

Integrative Taxonomy Reveals Molicola uncinatus and Gymnorhynchus gigas (Cestoda: Trypanorhyncha) Coinfection in the Atlantic Pomfret Brama brama From the Mediterranean Sea, With Notes on the Phylogenetic Position of G. gigas Within the Family Gymnorhynchidae

“…Morphological characters of the present specimens of M. uncinatus and G. gigas were in agreement with descriptions of Palm (2) and Casado et al (23,24). Molecular analysis confirmed the morphological identification of M. uncinatus being the sequences obtained identical to those of M. uncinatus previously collected in Thyrsites atun and L. caudatus (15,36). The sequences of G. gigas here obtained, revealing closer similarity with those of M. uncinatus, represent the first molecular data available for G. gigas, which should be considered a starting point for comparative analyses and molecular identification of this species.…”

“…Clades were considered to have high nodal support if the ML bootstrap resampling is ≥95%. The phylogenetic trees were rooted using Pintneriella musculicola Yamaguti, 1934 (15). For the phylogenetic tree construction, only the species with both 18S and 28S sequences were selected.…”

“…In both cases, Giarratana et al (10) and Panebianco et al (12) assumed that those larvae belonged to a single parasite species without even studying them. Recently, the application of molecular analyses for the identification of trypanorhynchs in Mediterranean fishes revealed that the larvae from the liver and muscles of the sunfish and the silver scabbardfish belonged to G. isuri (14) and M. uncinatus (15), respectively. This likely implies that the majority of the studies carried out so far from the Mediterranean Sea using questionable assumptions or morphological criteria alone for larvae identification reported misidentification of some Gymnorhynchidae species.…”

“…Nevertheless, misidentification of Gymnorhynchidae larvae using morphological criteria alone may occur because the isolation of their scoleces is difficult and often the partial or total invagination of their tentacles prevent the study of their most important taxonomic characteristics (2,3,14,15). When this occurs, the use of molecular analysis allows for species identification of trypanorhynch larvae that are challenging or not possible (14)(15)(16)(17). Correct identification of species is required to assess the biodiversity of an ecosystem.…”

A molecular and ecological study of Grillotia (Cestoda: Trypanorhyncha) larval infection in small to mid‐sized benthonic sharks in the Gulf of Naples, Mediterranean Sea

“…Understanding the factors that determine the occurrence or level of infection in marine fishes has interested scientists for decades and numerous variables about parasite, host, and environment have been identified as important in the dynamics of the host–parasite systems (Dallarés, 2016 ; Palm, 2004 ; Santoro, Iaccarino et al., 2020 ; Timi & Poulin, 2020 ; Tompkins et al., 2011 ). In particular, the probability to become infected with larval forms of trypanorhynchans, as well as their levels of infection, depends on a number of biotic and abiotic factors at different geographical scales (Palm, 2004 ; Palm et al., 2017 ; Palomba, Santoro et al., 2021 ; Santoro et al., 2020 ). The distribution of larval and adult parasites is generally shaped through biotic factors involved in transmission pathways, such as trophic interactions between definitive, intermediate, and transport hosts.…”