Functional Groups of Metazoan Parasites of the Dusky Flounder (Syacium papillosum) as Bioindicators of Environmental Health of the Yucatan Shelf.

We aimed to compare the percentage of explained variance given by the relationship of species and functional groups of metazoan parasites of the dusky flounder Syacium papillosum and environmental variables from water and sediments in the Yucatan shelf (YS). Parasite data were obtained from 127 S. papillosum specimens collected from 17 of 67 stations. At each station, 46 environmental variables were measured, including hydrocarbons, heavy metals, and physicochemical variables from water and sediments. Fifteen functional groups were defined based on biological characteristics of 48 parasite species. Our multivariate statistical analyses showed that species and functional groups produced similar explained variance values (47.3% and 50% respectively). However, using functional groups the time and financial resources were minimal compared with those used for morphological and molecular identification to produce the species composition matrix. Thus, functional groups are the best choice from the point of view of saving time and money.

The performance of taxonomic and trait-based approaches in the assessment of dusky flounder parasite communities as indicators of chemical pollution.

We assessed the performance of taxonomic and several functional trait-based approaches in the assessment of spatial and temporal patterns of dusky flounder (Syacium papillosum) parasite assemblages along the Yucatan shelf to determine their potential as bioindicators of marine chemical pollution. Fish specimens were collected throughout three research cruises that took place in 2015, 2016 and 2018. In addition to the traditional taxonomic approach, four trait-based approaches were performed including community-weighted means (CWM), functional trait niche (FTN), functional groups (FGs), and Rao's functional diversity (FD). Significant spatial and temporal variations in parasite communities were detected using the taxonomic approach. In general, these variations were also reflected in the four trait-based approaches performed, indicating that changes in taxa composition and abundance also resulted in functional composition shifts. Resemblance matrices of both taxonomic and functional trait approaches were significantly correlated. Variations in taxonomic and trait-based composition using the four approaches were significantly correlated with depth, and at least one chemical pollutant variable. Feeding mode, transmission, life stage and attachment structure displayed spatial variability and significant correlations with predictor variables, which indicates that this set of attributes functions as a good surrogate for assessing variations in the functional composition of flatfish parasite communities in relation to pollution. FTN and CWM were the approaches that best detected spatio-temporal variation. CWM and FD were best suited for detecting pollution gradients. These results reveal the feasibility of using trait-based approaches to assess marine parasite communities as bioindicators of chemical pollution. Functional traits of marine metazoan parasites are as good indicators of the effect of oil pollution as taxonomic diversity. This may be a time-saving and cost-effective approach to performing environmental assessments.

A new species of Neoheterobothrium Price, 1943 (Monogenea, Diclidophoridae) from Syacium papillosum (Linnaeus) (Pleuronectiformes, Paralichthyidae) in the Yucatan Shelf, with notes on the validity of the subfamilies in the Diclidophoridae.

Neoheterobothrium papillosum n. sp. (Monogenea: Diclidophoridae) is described based on specimens collected from the gills of the dusky flounder Syacium papillosum (Linnaeus) (Paralichthyidae) in the Yucatan Shelf. The new species can be differentiated from other congeneric species by the following characteristics: (1) number of hooks in the genital atrium (8 hooks), (2) number of testes (20-34), (3) pharynx size, (4) peduncle length, and (5) egg size. Neoheterobothrium papillosum n. sp. resembles Neoheterobothrium syacii; however, detailed morphological analysis allowed for their separation into two different species. Sequences of the nuclear ribosomal DNA partial 28S and ITS1 were obtained and compared with available sequences of other species and genera of the family Diclidophoridae from GenBank. A phylogenetic analysis was conducted, including 33 sequences, 18 of which represented 17 species and 11 genera of the family Diclidophoridae. The phylogenetic tree showed that Diclidophoridae is a monophyletic family and species of Diclidophora were grouped as the sister group of Neoheterobothrium papillosum n. sp. Our phylogenetic analyses were consistent with Mamaev's hypothesis, who divided Diclidophoridae into Diclidophorinae and Choricotylinae and concluded that Neoheterobothrium was a genus belonging to Diclidophorinae.

Phylogeny, genetics, and the partial life cycle of Oncomegas wageneri in the Gulf of Mexico.

Despite the diversity and ecological importance of cestodes, there is a paucity of studies on their life stages (i.e., complete lists of intermediate, paratenic, and definitive hosts) and genetic variation. For example, in the Gulf of Mexico (GoM) 98 species of cestodes have been reported to date; however, data on their intraspecific genetic variation and population genetic studies are lacking. The trypanorhynch cestode, Oncomegas wageneri, is found (among other places) off the American Western Atlantic Coast, including the GoM, and has been reported as an adult from stingrays and from several teleost species in its larval form (as plerocerci). This study represents the first report of 2 previously unregistered definitive hosts for O. wageneri, namely the Atlantic sharpnose shark Rhizoprionodon terraenovae and the southern stingray Hypanus americanus. In this work, partial sequences of the 28S (region D1-D2) ribosomal DNA were analyzed to include O. wageneri within an eutetrarhynchoid phylogenetic framework. All O. wageneri individuals (which included plerocerci and adults) were recovered as monophyletic and Oncomegas celatus was identified as the sister species of O. wageneri. Furthermore, population genetic analyses of O. wageneri from the southern GoM were carried out using DNA sequences of the mitochondrial cytochrome c oxidase subunit 1 (COI) gene, which reflected high genetic variation and a lack of genetic structure among the 9 oceanographic sampling sites. Based on these results, O. wageneri is panmictic in the southern GoM. More extensive sampling along the species entire distribution is necessary to make more accurate inferences of population genetics of O. wageneri.

Polycyclic aromatic hydrocarbons in the cestode Oncomegas wageneri parasite of Mexican flounder Cyclopsetta chittendeni.

The concentrations of polycyclic aromatic hydrocarbon metabolites (PAHm) and their bioconcentration factors (BCF) were determined in the larval stages of the cestode Oncomegas wageneri, recovered from the intestine of the Mexican flounder Cyclopsetta chittendeni, in the southern Gulf of Mexico. The PAHm concentrations in O. wageneri were measured using fixed-wavelength fluorescence spectrometry and compared with PAHm concentrations in host bile. Oncomegas wageneri PAHm concentrations were markedly higher than those in host tissues. The highest BCF values were obtained for 1-hydroxypyrene (OHP) and benzo(a)pyrene (BaP). Using a General Linear Model, a significant negative relationship was found between O. wageneri PAHm concentrations (as response variable) and the number of O. wageneri and oil well proximity. Low BCF values and PAHm concentrations in C. chittendeni correlated positively with O. wageneri PAHm concentrations. In contrast, high BCF values for PAHm concentrations in C. chittendeni had a negative association with O. wageneri PAHm concentrations. This study provides the first evidence of the presence of PAHm in intestinal larval cestodes of marine flatfishes, demonstrating levels of PAHm that were higher than levels in their hosts.

Parasitic nematodes of marine fishes from Palmyra Atoll, East Indo-Pacific, including a new species of Spinitectus (Nematoda, Cystidicolidae).

Here, we present the results of a taxonomic survey of the nematodes parasitizing fishes from the lagoon flats of Palmyra Atoll, Eastern Indo-Pacific. We performed quantitative parasitological surveys of 653 individual fish from each of the 44 species using the intertidal sand flats that border the atoll's lagoon. We provide morphological descriptions, prevalence, and mean intensities of the recovered seven species of adult nematode (Pulchrascaris chiloscyllii, Capillariidae gen. sp., Cucullanus bourdini, Cucullanus oceaniensis, Pseudascarophis sp., Spinitectus (Paraspinitectus) palmyraensissp. nov., Philometra pellucida) and three larval stages (Pulchrascaris sp., Hysterothylacium sp., Cucullanus sp.). We recorded: Pulchrascaris chiloscyllii from Carcharhinus melanopterus; Capillariidae gen. sp. from Chaetodon lunula, Lutjanus fulvus, and Ellochelon vaigiensis; Cucullanus bourdini from Arothron hispidus; Cucullanus oceaniensis from Abudefduf sordidus; Pseudascarophis sp. from Chaetodon auriga, Chaetodon lunula, and Mulloidichthys flavolineatus; Spinitectus (Paraspinitectus) palmyraensissp. nov. from Albula glossodonta; Philometra pellucida from Arothron hispidus; and three larval forms, Pulchrascaris sp. from Acanthurus triostegus, Acanthurus xanthopterus, Rhinecanthus aculeatus, Platybelone argalus, Carangoides ferdau, Carangoides orthogrammus, Caranx ignobilis, Caranx melampygus, Caranx papuensis, Chaetodon auriga, Chanos chanos, Amblygobius phalaena, Asterropteryx semipunctata, Valencienea sexguttata, Kyphosus cinerascens, Lutjanus fulvus, Lutjanus monostigma, Ellochelon vaigiensis, Mulloidichthys flavolineatus, Upeneus taeniopterus, Gymnothorax pictus, Abudefduf septemfasciatus, Abudefduf sordidus, and Stegastes nigricans; Hysterothylacium sp. type MD from Acanthurus triostegus, Carangoides ferdau, Chaetodon lunula, Chanos chanos, Kyphosus cinerascens, Abudefduf sordidus, and Arothron hispidus; and Cucullanus sp. from Caranx ignobilis. Spinitectus (Paraspinitectus) palmyraensissp. nov. (Cystidicolidae) is described from the intestine of roundjaw bonefish Albula glossodonta. All the nematode species reported in this study represent new geographical records. We discuss how our survey findings compare to other areas of the Indo-Pacific, and the way the relatively numerical dominance of trophically transmitted larval stages likely reflect the intact food web of Palmyra Atoll, which includes a large biomass of large-bodied top predator sharks and ray-finned fishes.

Metazoan parasite infracommunities of the dusky flounder (Syacium papillosum) as bioindicators of environmental conditions in the continental shelf of the Yucatan Peninsula, Mexico.

BACKGROUND: We assessed metrics of the metazoan parasite infracommunities of the dusky flounder (Syacium papillosum) as indicators of aquatic environmental health of the Yucatan Shelf (YS) prior to oil extraction. We sampled the dusky flounder and its parasites along the YS, mostly during the 2015 north wind season (November-April). Our aims were: (i) to determine whether the parasite infracommunity metrics of S. papillosum exhibit significant differences among YS subregions; (ii) to determine whether the probability of the occurrence of its parasite species and individuals were affected by environmental variables, nutrients, heavy metals and hydrocarbons at the seascape level; and (iii) to determine whether there were statistical differences between the parasite infracommunity metrics of S. papillosum from YS and those of Syacium gunteri from the Campeche Sound. Multivariate statistical analyses and generalised additive models (GAMs) were used to examine the potential statistical associations between the contaminants, environmental variables and parasite community metrics, and the maximum entropy algorithm (MaxEnt) was used to characterise the habitat's suitability for the parasite's probability of occurrence. RESULTS: We recovered 48 metazoan parasite species from 127 S. papillosum, with larval cestodes and digeneans being the most numerically-dominant. Multivariate analyses showed significant differences in parasite infracommunity metrics among Western YS, Mid YS and Caribbean subregions, with the latter being the richest in species but not in individuals. The GAM and MaxEnt results indicated a negative effect of top predators (e.g. sharks and rays) removal on parasite metrics. The parasite infracommunities of S. papillosum were twice as rich in the number of species and individuals as those reported for S. gunteri from the Campeche Sound. CONCLUSIONS: The significant differences among subregions in parasite metrics were apparently due to the interruption of the Yucatan current during the north wind season. The fishing of top predators in combination with an influx of nutrients and hydrocarbons in low concentrations coincides with an increase in larval cestodes and digeneans in S. papillosum. The dusky flounder inhabits a region (YS) with a larger number of metazoan parasite species compared with those available for S. gunteri in the Campeche Sound, suggesting better environmental conditions for transmission in the YS.

Parasitic copepods (Crustacea, Hexanauplia) on fishes from the lagoon flats of Palmyra Atoll, Central Pacific.

We surveyed copepods parasitic on the fishes at Palmyra, a remote atoll in the Central Indo-Pacific faunal region. In total, we collected 849 individual fish, representing 44 species, from the intertidal lagoon flats at Palmyra and recovered 17 parasitic copepod species. The parasitic copepods were: Orbitacolaxwilliamsi on Mulloidichthysflavolineatus; Anuretesserratus on Acanthurusxanthopterus; Caligusconfusus on Carangoidesferdau, Carangoidesorthogrammus, Caranxignobilis, Caranxmelampygus, and Caranxpapuensis; Caliguskapuhili on Chaetodonauriga and Chaetodonlunula; Caliguslaticaudus on Rhinecanthusaculeatus, Pseudobalistesflavimarginatus, M.flavolineatus, Upeneustaeniopterus, Chrysipteraglauca, and Epinephalusmerra; Caligusmutabilis on Lutjanusfulvus and Lutjanusmonostigma; Caligusrandalli on C.ignobilis; Caligus sp. on L.fulvus; Caritusserratus on Chanoschanos; Lepeophtheiruslewisi on A.xanthopterus; Lepeophtheirusuluus on C.ignobilis; Dissonussimilis on Arothronhispidus; Nemesis sp. on Carcharhinusmelanopterus; Hatschekialongiabdominalis on A.hispidus; Hatschekiabicaudata on Chaetodonauriga and Chaetodonlunula; Kroyerialongicauda on C.melanopterus and Lernanthropus sp. on Kyphosuscinerascens. All copepod species reported here have been previously reported from the Indo-Pacific but represent new geographical records for Palmyra, demonstrating large-scale parasite dispersion strategies.

Rapid infection and proliferation of dactylogyrid monogeneans on gills of spotted rose snapper (Lutjanus guttatus) after transfer to a sea-cage.

Finfish mariculture is typically threatened by parasite and disease outbreaks. Therefore, it is important to identify parasite species of potential risk for this activity. Snappers are valuable food fish worldwide. In the Eastern Pacific, spotted rose snapper (Lutjanus guttatus [Steindachner, 1869]) is a firm candidate for sea-cage aquaculture. In the current study, the parasitism of caged L. guttatus by dactylogyrids was evaluated for the first time during a complete farming period. Twenty five thousand juvenile fish produced at the Research Center for Food and Development (CIAD, Mazatlan Unit) were reared in a sentinel sea-cage from February to November 2012 in Mazatlan Bay, Mexico. A fish sample (n=15) was obtained every month. Dactylogyrids from the left second gill arch were identified and quantified. A total of 18,704 dactylogyrids distributed in three species, Euryhaliotrema perezponcei García-Vargas, Fajer-Ávila and Lamothe-Argumedo, 2008, E. mehen (Soler-Jiménez, García-Gasca and Fajer-Ávila, 2012), and Haliotrematoides guttati García-Vargas, Fajer-Ávila and Lamothe-Argumedo, 2008 (Monogenea: Dactylogyridae) was found, which were able to infect caged L. guttatus since the first month of the farming period. Prevalence of these parasite species was 100% all the time, except for initial low values for E. mehen and H. guttati. The mean intensity of infection of each dactylogyrid species varied significantly between sampling months. Euryhaliotrema perezponcei was the most abundant parasite, reaching the highest mean intensity in May, June and July (154.3, 296.9 and 176.6 parasites/host, respectively). No clear seasonality of infection was observed; however, the influence of the water temperature on the observed infection levels is discussed. There was no mortality, change on behavior or pathological signs. However, given the rapid infection and proliferation of dactylogyrids, particularly E. perezponcei on L. guttaus reared in a sentinel sea-cage, outbreak of these parasites could be expected when this fish species is cultured on a large scale.

A new species of Euryhaliotrematoides Plaisance & Kritsky, 2004 (Monogenea: Dactylogyridae) from the gills of the spotted rose snapper Lutjanus guttatus (Steindachner) (Perciformes: Lutjanidae).

Euryhaliotrematoides mehen n. sp. (Monogenea: Dactylogyridae) is described based on specimens collected from the gills of the spotted rose snapper Lutjanus guttatus (Steindachner) off Mazatlan, Sinaloa, on the northwestern coast of Mexico. The synapomorphy of this genus is the presence of a funnel-shaped base of the male copulatory organ. This new species differs from all other species of the genus by possessing a male copulatory organ with a base with a thickened margin and a membranous accessory piece resembling a scarf and covering about 60% of its distal region. PCR products of the 28S rRNA (831 bp) and 18S rRNA (662 bp) genes were sequenced and submitted to GenBank (accession numbers HQ615997 and JF938069, respectively). BLASTn searches revealed no 100% identical hits with the previously registered monogenean sequences.

The microecology of dactylogyrids (Monogenea: Dactylogyridae) on the gills of wild spotted rose snapper Lutjanus guttatus (Lutjanidae) from Mazatlan Bay, Mexico.

The spatial distribution and coexistence of monogenean dactylogyrids was assessed on the gills of 63 specimens of wild spotted rose snapper, Lutjanus guttatus (Steindachner), caught in the Mazatlan Bay, Sinaloa, Mexico. Five species are reported: Euryhaliotrema perezponcei Garcia-Vargas, Fajer-Avila et Lamothe-Argumedo, 2008, Euryhaliotrematoides sp., Haliotrematoides spinatus Kritsky et Mendoza-Franco, 2009, H. plectridium Kritsky et Mendoza-Franco, 2009, and H. guttati Garcia-Vargas, Fajer-Avila et Lamothe-Argumedo, 2008. All except E. perezponcei and H. guttati represent new geographical records for the Pacific coast. The most prevalent dactylogyrid species was E. perezponcei (100%), H. plectridium and H. spinatus had > 80% prevalence, and H. guttati and Euryhaliotrematoides sp. had the lowest prevalence. The mean abundance of H. plectridium and E. perezponcei was close to 60 parasites/fish, whereas Euryhaliotrematoides sp. and H. guttati had the lowest abundance. The dactylogyrid species exhibited a tendency for attachment to gill arch 2: 25% attachment occurring on gill arch 1, 30% on 2, 27% on 3 and 18% on 4, and showed a significant preference for the central sector of the gill (42%). Haliotrematoides plectridium had a preference for attachment to gill arches 2 and 3 and the central sector. Haliotrematoides spinatus tended to settle on the gill arches 2 and 3 and had a preference for the central sector. Euryhaliotrema perezponcei tended to settle on the gill arches 1 and 2 and the anterior gill sector. Euryhaliotrematoides sp. and H. guttati did not show a preference for any gill arch or sector. The intraspecific aggregation was stronger than the interspecific aggregation, indicating that all the dactylogyrid species on spotted rose snapper were aggregated, and there was no evidence of competition among the species.