Open-access New host records of parasitic isopods of Tropical Eastern Pacific marine fishes, with remarks on the taxonomy and distribution of the species

Abstract

Marine fishes harbor a wide array of metazoan parasites, including helminths and crustaceans such as copepods and isopods. Even though the coast of Sinaloa stands out in Mexico by the volume of captured marine fishes, information about the diversity of their parasites is still very scarce. Isopods belonging to the families Cymothoidae, Gnathiidae, Corallanidae, and Aegidae are composed of temporary or obligate ectoparasites of the skin, gills, gill-chamber, or mouth of marine fishes across the world. In this study, we report data on the presence of isopods of the families Cymothoidae, Gnathiidae, and Aegidae infecting fishes from three localities at Sinaloa, Mexico. Fishes were obtained from commercial capture and the body surface, gill chamber, and mouth were examined for parasitic isopods. We report five parasitic isopod taxa in 16 fish host species, including Ceratothoa gilberti (Richardson, 1904), Nerocila californica Schioedte and Meinert, 1881, a potential new species identified as Cymothoa sp. A, Rocinela signata Schioedte and Meinert, 1879, and praniza and zuphea larvae of Gnathiidae species. Also, we compiled information on previous records of these species in marine fishes along the Mexican Pacific coast and discussed the importance of our findings for understanding the diversity and distribution patterns of these ectoparasites in the Southeastern Gulf of California.

Keywords:
Crustacean; Gulf of California; marine fishes; metazoan parasites; Mexican Pacific

INTRODUCTION

Fish parasites play an essential role in aquatic ecosystems since they can regulate host populations and influence biological traits of the host such as reproduction, behavior, and even migratory patterns (Luque and Poulin 2007; de Souza et al., 2019). Additionally, some parasites may cause public health problems due to the risk of zoonotic diseases (Shamsi and Barton, 2023). Metazoan parasites, including helminths and crustaceans commonly parasitize marine fishes. Among the latter, isopods are very important. Approximately 10,687 isopod species included in 1,557 genera and 141 families have been described thus far of which 1,486 are parasitic (Hartebrodt et al., 2023). Among parasitic forms, cymothoid isopods are obligate fish parasites, occurring in all oceans except polar waters (Smit et al., 2014; 2019) as ectoparasites on the body surface, buccal cavity, gill chamber, and some species are found under the host epidermis (Bunkley-Williams and Williams, 1998), causing severe tissue damage and mortality (de Souza et al., 2019; Vigneshwaran et al., 2019; Smit et al., 2019; Mahmoud et al., 2023). Parasitic isopods are of major concern when infesting fish during aquaculture activities (Horton and Okamura, 2001; Fadel et al., 2020; Piazzon et al., 2021; Abdallah and Hamouda, 2022) by producing a severe effect on fish growth and gonad development (Cong et al., 2017; Muniesa et al., 2020), causing economic losses (Mladineo et al., 2020; Hadfield and Smit, 2020).

In Mexico, some studies have reported the presence of cymothoid isopods parasitizing marine fishes. For instance, Brusca (1981) reported 14 cymothoid species across the eastern Pacific coast of which 11 are from Mexican waters: Anilocra laticauda H. Milne Edwards, 1840; Ceratothoa gilberti (Richardson, 1904); Ceratothoa gaudichaudii (H. Milne Edwards, 1840) (taxon inquirendum); Cymothoa exiguaSchioedte and Meinert, 1884; Elthusa californica (Schioedte and Meinert, 1884); Elthusa menziesi (Brusca, 1981); Elthusa vulgaris (Stimpson, 1857); Livoneca bowmaniBrusca, 1981; Nerocila californicaSchioedte and Meinert, 1881; Renocila thresherorumWilliams and Bunkley-Williams, 1980, and Smenispa convexa (Richardson, 1905). Espinosa-Pérez and Hendrickx (2001; 2006) added three species of Cymothoidae: Mothocya gilliBruce, 1986; Mothocya rosea Bruce, 1986, and Mothocya arrosor Bruce, 1986, and six species of Aegidae: Aegiochus plebeiaHansen, 1897; Rocinela belliceps (Stimpson, 1864); Rocinela laticaudaHansen, 1897; Rocinela murilloiBrusca and Iverson, 1985; Rocinela signata Schioedte and Meinert, 1879, and Rocinela tuberculosaRichardson, 1898. Finally, Bruce and Bowman (1989) reported Glossobius auritusBovallius, 1885, an Indo-Pacific species on the coast of Guerrero, Mexico.

Particularly, on the coast of Sinaloa, several studies contributed to the metazoan parasite biodiversity of marine fishes, particularly for helminths and copepods (see Grano-Maldonado and Pérez-Ponce de León, 2023a; 2023b, and references therein). However, parasitic isopods have been scarcely studied in this region. Only four species of Cymothoidae have been reported, including L. bowmani, N. californica, Ce. gilberti, and M. gilli (see Bruce, 1986; Alvarez-León, 1981; Grano-Maldonado et al., 2024). The main objective of this study is to report new host records of parasitic isopods of marine fishes from the coast of Sinaloa and provide additional information on the taxonomy and geographic distribution of the species across the Tropical Eastern Pacific.

MATERIAL AND METHODS

Isopod specimens were obtained from marine fishes sampled randomly between October 2018 and January 2024. Fishes were collected by local fishermen in the littoral zone (< 20 m depth) from three localities: off Mazatlán, Sinaloa, in the Urias estuary, Mazatlán, and off Marmol, a locality about 35 km NW of Mazatlán (Fig. 1). Fish were kept on ice and transported to the laboratory for a parasitological examination. The mouth, eyes, fins, skin, and gill cavity of each host were carefully examined for ectoparasites. Parasites were removed, relaxed in marine water, and fixed in 96% alcohol. The total length (TL) of isopods is expressed in millimeters (mm). Fish species were identified using general keys (Fischer et al., 1995a; 1995b; Thomson et al., 2000). The isopods were identified according to the group reviews carried out by different authors (e.g., Brusca, 1981; Bruce, 1986; Brusca and France, 1992; Hadfield et al., 2016). The composite digital images of the specimens were made with a Canon Powershot S3 IS digital camera attached to a Steami 2000 stereomicroscope. Between 5-15 photographs were taken at different focal planes and combined using Combine ZP-Free image stacking software for depth of field correction (Hadley, 2011). Most specimens were deposited in the Regional Collection of Marine Invertebrates of the Instituto de Ciencias del Mar y Limnología, UNAM, in Mazatlán. The accession numbers to the Regional Collection (ICML-EMU) are indicated in “Material examined” section of each species description.

Figure 1.
Localities from the Sinaloa state where the fish species indicated in this study were collected. (The numbers correspond to: 1, Urías Estuary; 2, Mazatlán Bay; 3, Mármol).

RESULTS

Five taxa of parasitic isopods belonging to three families: Cymothoidae (C. gilberti, N. californica and Cymothoa sp. A), Aegidae (R. signata), and Gnathiidae (Gnathiidae species), were found in 15 fish species belonging to 11 families (Ariidae, Balistidae, Belonidae, Carangidae, Gerridae, Lutjanidae, Mugilidae, Monacanthidae, Polynemidae, Sciaenidae, Serranidae) (Tab. 1).

Table 1.
Host records of isopods from marine fishes reported in this study and previous records from literature. Species marked with asterisk (*) represent new host records.

SYSTEMATICS

Order Isopoda Latreille, 1817

Suborder Cymothoida Wägele, 1815

Family Cymothoidae Leach, 1814

Ceratothoa gilberti ( Richardson, 1904 )

(Fig. 2)

Figure 2.
Ceratothoa gilberti (ICML-EMU 13783). Female from the buccal cavity of Mugil cephalus (Mugilidae), Jun 7, 2018, Mazatlán.

Material examined. Boca del Caimanero, Mazatlán. Jun 7, 2018, 1 female (TL 16.5) in the buccal cavity and 1 male (TL 8.7) in the gill chamber of Mugil cephalus (Mugilidae), (ICML-EMU 13783).

Distribution. From SW California to Mazatlán, including the Gulf of California (see Hadfield and Smit, 2020).

Previous known hosts. Mugil cephalus and Mugil hospes (see Hadfield and Smit, 2020).

Remarks. According to Brusca (1981), the genus CeratothoaDana, 1852 and CymothoaFabricius, 1793 are two of the most common genera of tongue-biters (cymothoids found inside the buccal-cavity of fish). According to Hadfield et al. (2014), species of Ceratothoa can be easily identified by the presence of a triangular cephalon, contiguous antennular bases, pleonite 1 narrower than the other pleonites, and an elongate body (2.1-2.9 times as long as wide). Ceratothoa gilberti is easily distinguished from the other Ceratothoa species because it is the only species without a considerable expansion at the base of the latter pereopods 5-7 (Bruce and Bowman, 1989). According to Brusca (1981) and Espinosa-Perez and Hendrickx (2001), only two species of Ceratothoa have been found on the eastern Pacific coast, Ce. gilberti and Ce. gaudichaudii (species inquirenda).

In a comprehensive review of the fish hosts of Ce. gaudichaudii elaborated by Muñoz and Olmos (2007), the authors mentioned that the species has been found in the buccal cavity, branchial arches, and gill chamber of 14 fish species of elasmobranch and teleost fishes. However, none of those species belongs to the family Mugilidae and Ce. gilberti has only been found infesting Mugilids (Hadfield and Smit, 2020).

Nerocila californica Schioedte and Meinert, 1881

(Fig. 3)

Figure 3.
Nerocila californica (ICML-EMU 13785-A). Female from the skin of Bagre panamensis (Ariidae), Oct 13, 2023, Urías estuary.

Material examined. Boca del Asadero, Nayarit, Nov 28, 2019, 21 females (TL 14.8-21.6) and 1 male (TL 12.9), caudal fin of Micropogonias altipinnis (Sciaenidae) (ICML-EMU 13784). Urías estuary: Oct 13, 2023, 3 females (TL 15-18.9) on Bagre panamensis (Ariidae) (ICML-EMU 13785-A). Off Mazatlan bay: Ago 12, 2023, 2 females (TL 22.8-24) on caudal fin of M. altipinnis (ICML-EMU 13785-B); Ago 27, 2023, 5 females (TL 12.0-16.8), fins of B. panamensis (ICML-EMU 13785-C); Ago 27, 2023,1 female (TL16.5), on Ophoioscion scierus (Sciaenidae) (ICML-EMU 13785-D); Oct 9, 2023, 4 females (TL 14.2-18.5), on Hoplopagrus guentherii (Lutjanidae) (ICML-EMU 13785-E); Oct 14, 2023, 2 males (TL 10.1-12.3) on fins of B. panamensis, (ICML-EMU13785-F); Dec 8, 2023, 25 females (TL 14.6-21.7) and 2 males (TL 12.0-12.3), on caudal fin of M. altipinnis, (ICML-EMU 13786); Dec 13, 2023, 5 females (TL 14-15.7), on B. panamensis (ICML-EMU 13785-G); Dec 20, 2023, 2 females (TL 17.1), on B. panamensis (ICML-EMU 13785-H); Jan 12, 2024, 2 females (TL 15.2-19.8) on B. panamensis; Jan 12, 2024, 2 females (TL 15.2-16.5) on Polydactylus opercularis (Polynemidae) (ICML-EMU 13785-I). Additional record: Off Mazatlán Bay Mar 28, 2023, 1 female was observed on the dorsal fin of Aluterus monoceros (Monacanthidae).

Distribution. California, from the Gulf of California to Ecuador and the Galapagos Islands.

Previous known hosts. About 45 host fish species of 20 families (see Brusca, 1981; Del Moral-Flores et al., 2020).

Remarks. Most of the reports of Nerocila in the Eastern Pacific had been referred to N. acuminata (e.g. Brusca, 1981), although those records are currently attributed to N. californica (Segal, 1987; Del Moral-Flores et al., 2020); this contention is supported by Boyko et al. (2024) who showed that the distribution of N. acuminata is restricted to the western Atlantic coast, with the vast majority of records across the Gulf of Mexico; instead, the distribution of N. californica extends from California, including the Gulf of California, to the Galapagos Islands. In this study, most of the specimens of N. californica were collected from the caudal fin of the fishes, especially on B. panamensis captured off Mazatlán and the Urías estuary; the highest parasite loads were recorded from the caudal fin of two specimens of M. altipinnis (21 and 27 parasites). In our study, we added M. altipinnis, B. panamensis, H. guentherii, A. monoceros, P. opercularis, and O. scierus as new hosts of N. californica (Tab. 1).

Cymothoa sp. A

(Fig. 4)

Figure 4.
Cymothoa sp. A (ICML-EMU 13774). Female from the buccal cavity of Lutjanus aratus (Lutjanidae) Oct 13, 2018, Off Mazatlán Bay.

Material examined. Off Mazatlán Bay: Oct 13, 2018, 1 female (TL 32.5), in the buccal cavity of Lutjanus aratus (Lutjanidae) (ICML-EMU 13774); Oct 16, 2023, 1 female (TL 24.2), in buccal cavity and 1 male (TL 15.7) in gill chamber of Lutjanus peru (ICML-EMU 13779).

Previous known hosts. None

Distribution. Only known from off Mazatlán.

Remarks. Until now, the only known species of Cymothoa on the Eastern Pacific coast is Cy. exigua. The specimens we sampled from Sinaloa differ from Cy. exigua. The main morphological differences are found in the eyes, pereon, pereopods, and telson. The most obvious difference is that in Cy. exigua the lateral margins of the pereonite 7 reach the anterior margin of the pleotelson (see Brusca, 1981: 188, fig. 25) whereas in our specimens the last pereonite is not so curved and the lateral margins only reach the lateral margins of the first or second pleonites (Fig. 4). Our specimens also resemble morphologically the species Cymothoa excisaPerty, 1833 which is distributed on the western Atlantic. Still, both species can be easily separated because in Cy. excisa the fourth pereonite is as long as the first one, and the distal margin of the telson is continuous (see Thatcher et al., 2003: 545, figs. 27, 28); instead, in Cymothoa sp. A the pereonites 2-4 are similar in length and the pleotelson has a medial distal notch (Fig. 4). We are certain that our specimens represent an undescribed species. A more detailed description of this species is currently in preparation.

Family Aegidae White, 1850

Rocinela signata Schioedte and Meinert, 1879

(Fig. 5)

Figure 5.
Rocinela signata (EMU 13780). Female from the gills of Lutjanus argentiventris (Lutjanidae) Mar. 3, 2023, Off Mazatlán Bay.

Material examined. Mazatlán Bay, Mar. 3, 2023, 1 female (TL 4.6), gills of Lutjanus argentiventris (Lutjanidae) (EMU 13780); 2 females (TL 7-10), gills of H. guentherii. Sep. 20, 2023, 2 females (TL10.4-11.4), gills of H. guentherii. Nov. 4, 2023, 1 female (TL 15.3), gills Eucinostomus currani (Gerridae). Nov. 8, 2023, 1 female (T.L. 13.1), gills Balistes polylepis (Balistidae).

Distribution. California, U.S.A., to Ecuador and Galapagos Islands (Brusca and France, 1992).

Previous known hosts. In the Eastern Pacific, Anisotremus interruptus (Haemulidae), Mycteroperca jordani (Serranidae), Parapsettus panamensis (Ephippidae), Euthynnus lineatus (Scombridae), Scomberomorus sierra (Scombridae), Caranx sexfasciatus, Caranx caninus, Caranx caballus, Caranx vinctus, Chloroscombrus orqueta, S. peruviana, Hemicaranx leucurus (Carangidae), H. guentherii and L. guttatus (Lutjanidae) (Brusca and France, 1992; Miranda-Delgado et al., 2019; Santos-Bustos et al., 2020a; Violante-González et al., 2016; 2020; Villalba et al., 2022; Osuna-Cabanillas et al., 2024).

Remarks. According to Brusca and France (1992), Ro. signata can be distinguished from the other species of Rocinela by having a long medial process of the uropodal peduncle (more than 70% of the uropod length), distal margin of pereonites smooth, and the propod of pereopods I-III not medially expanded with only 1 or 2 minute spiniform setae. Another character considered reliable for the identification of R. signata is the presence of a chromatophore pattern similar to an inverted “W” on the dorsum of the pleotelson (Moreira, 1972; Cardoso et al., 2017; Aguilar-Perera and Noh-Quiñonez, 2022). The specimens we sampled correspond with the description of Ro. signata given by Brusca and France (1992), however, only two of the six specimens of our study had a “W”-like pattern of chromatophores on the pleotelson (Fig. 5b). Brusca and France (1992) had already pointed out that the chromatophore pattern was not constant among nearly 60 of the specimens from the Eastern Pacific they observed. Moreover, if the presence of Ro. signata in the Eastern Pacific is not the result of its introduction in relatively recent times, its amphi-American distribution is, at least, suspicious. In this context, Baddour et al. (2024) refer to a case of parasitism of Ro. signata on Fistularia commersonii (Fistulariidae) in Syria although they support their identification with a poor description and the presence of an inverted “W” in the pleotelson of the isopods. We cannot rule out that the presence of “Ro. signata” in Syria was a case of an introduction of the species in that region, but we consider that a key identification of this species based on the pigmentation of the pleotelson could be erroneous. The variations in the body parts and chromatophore patterns of the specimens reported as Ro. signata lead us to think that the wide distribution of this species could represent a species complex. A detailed study and the comparison of individuals from different populations, based on both, morphological and molecular analysis, is desirable to assess the taxonomic status of this species.

Gnathiidae species

(Fig. 6)

Figure 6.
Gnathiidae species. A, B: Praniza larvae; C: zuphea larva, collected from gills of Hoplopagrus guentherii; Mazatlán Bay, Sep. 13, 2023.

Material examined. Mazatlán Bay: Sep. 13, 2023, 12 praniza larvae (TL 2.4-2.6), on gills of H. guentherii; Oct 8, 2023 29 praniza larvae (TL 1.8-2.1) on gills of E. currani; Jun 6, 2022 8 praniza larvae (TL 2.2-2.3) on gills of B. polylepis; Nov. 28, 2023, 153 praniza larvae (TL 2.3-2.6), on gills of Ephinephelus labriformis (Serranidae); Oct. 12 2023, 85 praniza larvae (TL 1.9-2.3), on gills of L. guttatus; Nov 5, 2023, 85 praniza larvae (TL 2.4-2.7), on gills of M. cephalus; Nov 12, 2023 383 pranizas larvae (TL 2.1-2.6),on gills of Diapterus peruvianus (Gerreidae); Feb 07, 2024 33 pranizas larvae (TL 2.0-2.4), on gills of Tylosurus pacificus (Belonidae).

Distribution. Mazatlán Bay.

Previous known hosts. In the Eastern Pacific, Caranx caninus, Caranx caballus, Caranx vinctus, Selene brevoortii (Carangidae); P. panamensis; Euthynnus lineatus, and Sarda orientalis (Scombridae) (Violante-González et al., 2016; 2020; Miranda-Delgado et al. 2019; Villalba-Vázquez et al., 2018; Santos-Bustos et al., 2020b; and Osuna-Cabanillas et al., 2024). All these records were made as Gnathia sp.

Remarks. At least seven studies on marine fish parasites along the Mexican Pacific coast have reported the presence of the praniza larva of Gnathia sp. (Violante-González et al., 2016; 2020; 2023; Villalba-Vázquez et al., 2018; Miranda-Delgado et al., 2019; Santos-Bustos et al. 2020b; Osuna-Cabanillas et al., 2024). However, we acknowledge that the taxonomic identification of gnathiids is based on the free-living adult forms (Hadfield et al., 2009). We were unable to associate the praniza and zuphea larvae of the family Gnathiidae with adults of any known species. The identification of these isopods is based on the morphology of the adult males, and this is challenging as males can be difficult to obtain (Smit and Davies, 2004). Only free-living adults of the species Gnathia steveniMenzies, 1962 have been recorded along the Pacific coast of Mexico, particularly in Bahia San Quintin, west Baja California (Espinosa- Pérez and Hendrickx, 2002). The presence of such larvae in the five species of fish reported in this study in Mazatlán represents new host and locality records for this group of isopods (Tab. 1).

DISCUSSION

Studies on the isopod parasite fauna of marine fishes are relatively scarce in Mexico, considering records made along the Pacific coast, the Gulf of Mexico, and the Caribbean Sea (Brusca, 1981; Espinosa-Pérez and Hendrickx, 2001; 2006; see also Aguilar-Perera, 2022). Our study provides new information on the host and distribution records for five parasitic isopod taxa infesting 16 fish species. Aguilar-Perera (2022) recently published a checklist of the parasitic isopods of marine decapods and fishes off Mexico’s coasts. The author reported 33 parasitic isopod species, with 24 of them belonging to the family Bopyridae (infesting 30 decapod species), and only nine species of the families Aegidae, Ancinidae, and Cymothoidae (infesting 18 fish species). However, the checklist is not comprehensive since the author did not list all the records available in the literature. For instance, Aguilar-Perera (2022) did not include 17 species of parasitic isopods in marine fish belonging to the families Aegidae (Ae. plebeia, Ro. belliceps, Ro. laticauda, Ro. murilloi, and Ro. tuberculosa) and Cymothoidae (An. laticauda, Ce. gilberti, Ce. gaudichaudii, E. californica, E. menziesi, E. vulgaris, L. bowmani, Re. thresherorum, S. convexa, M. gilli, M. rosea and M. arrosor), as reported by Brusca (1981) and Espinosa-Pérez and Hendrickx (2006).

Aguilar-Perera (2022) further discussed that the cymothoid species reported in his checklist were reported in fish hosts from the southern Gulf of Mexico with seven species, and Mexican Pacific with two species, although the list includes five species for the Pacific coast. Clearly, the checklist is incomplete. In addition to that, some reports have been published after Aguilar-Perera (2022) and the distributional range and host species of some parasitic isopods has been expanded. For instance, Violante-González et al. (2023) reported Rocinela cf. hawaiiensis from Lutjanus inermis in Acapulco; Grano-Maldonado et al. (2024) reported M. gilli from Hyporamphus naos in Mazatlán, and Osuna-Cabanilla et al. (2024) reported Ro. signata and the larvae of Gnathia sp. as parasites of C. caballus from the same locality.

Still, a molecular study, or a life cycle study under controlled conditions, would be required to establish a link between larval forms and adults as Gnathiidae species. The identification of gnathiid larvae in marine fishes as members of the genus Gnathia is challenging and requires further analyses; the studies reporting the presence of such larvae mentioned above did not conduct such analyses and in consequence, those records are doubtful and require further verification. In this study, we took a conservative position and the praniza and zuphea larvae found in several host species in Sinaloa were identified as Gnathiidae species.

The addition of an undescribed species of Cymothoa in our study then raises the number of parasitic isopods in marine fishes along the Pacific coast of Mexico to 22 species. It is interesting to note that only one species of parasitic isopod was previously accepted as valid for the Pacific coast, Cy. exigua. In our study, we discovered that the specimens sampled in lutjanids of Sinaloa are distinct from Cy. exigua; however, they will be described in a separate paper. Still, we argue that some morphological characters commonly used to diagnose species in the genus Cymothoa require a detailed morphological and morphometrical analysis. For example, differences are found between these two species in the shape and size of the eyes, pereon, pereopods, and telson, but the shape and extension of the lateral margins of the pereonite 7 are very important to separate them. Further studies describing the diversity and distribution patterns among species of Cymothoa will require in addition, strategic sampling, as pointed out by Tavares-Dias and Oliveira (2024). These authors proposed that a full understanding of Cymothoa diversity not only needs the collection of individuals in under-sampled regions but also the screening of non-commercial fish species. Our study shows that detailed morphometrical analyses of the specimens in tropical latitudes may lead to the discovery of new species.

Smit et al. (2014) described the large-scale biogeographical pattern of a latitudinal gradient of species diversity in cymothoid isopods. Species diversity decreases from the tropics to the cold waters and, based on the available data, the authors considered regions such as seaboards of the South Atlantic, the Eastern and Western Indian Ocean, and the Eastern Indo-Pacific poorly sampled for parasitic isopods. Our results show that the Eastern Tropical Pacific should also be considered one of the major regions where the documentation of parasitic isopod fauna remains minimal. The results of our study also reveal that the inventory of the parasitic isopods of marine fishes of Mexico is far from complete. Overall, the description of parasite diversity still requires the study of a larger number of host species from different localities. We pose that future studies on the metazoan parasite fauna of marine fishes in this geographic region will reveal an increase in species diversity of parasitic isopods.

ACKNOWLEDGMENTS

We thank fishermen from Playa Norte and Isla de la Piedra, Mazatlán, who helped to provide fish for this study; and Vicente Hernández and Roberto Paredes for their support in fish sampling (IMIPAS, CRIAP-Mazatlán). We are grateful to curators and collection managers for providing access to the material (ICML, UNAM) in Mazatlán. We extend our gratitude to the anonymous reviewers for their kind comments on improving our manuscript. We thank the social services students for helping with the sampling.

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  • Consent for publication
    All authors declare that they have reviewed the content of the manuscript and gave their consent to submit the document.
  • Data availability
    All study data are included in the article and/or supplementary material.
  • Funding and grant disclosures
    Not applicable.
  • Study permits
    Not applicable because fish samples were obtained from commercial capture.

Edited by

  • Associate Editor:
    Breda Doti
  • Editor-in-chief:
    Christopher Tudge

Data availability

All study data are included in the article and/or supplementary material.

Publication Dates

  • Publication in this collection
    11 July 2025
  • Date of issue
    2025

History

  • Received
    26 Apr 2024
  • Accepted
    08 Oct 2024
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