Ana Pérez-del-Olmo

Molecular and morphological evidence for three species of Diplostomum (Digenea: Diplostomidae), parasites of fishes and fish-eating birds in Spain

BackgroundRecent molecular studies have revealed high species diversity of Diplostomum in central and northern Europe. However, our knowledge of the distribution of Diplostomum spp. in the southern distributional range in Europe of the snail intermediate hosts (Lymnaea stagnalis and Radix spp.) is rather limited. This study aims to fill this gap in our knowledge using molecular and morphological evidence.MethodsNineteen fish species and six fish-eating bird species were sampled opportunistically in three regions (Catalonia, Extremadura and Aragon) in Spain. All isolates of Diplostomum spp. were characterised morphologically and molecularly. Partial sequences of the barcode region of the cox 1 mitochondrial gene and complete sequences of the ribosomal ITS1-5.8S-ITS2 gene cluster were used for molecular identification of the isolates.ResultsIntegrated morphological and molecular analyses demonstrated the presence of three species among the larval and adult isolates of Diplostomum spp. sampled in Spain: Diplostomum spathaceum (in fish and birds), D. pseudospathaceum (in birds) and Diplostomum sp. (in fish) referred to as Clade Q sensu Georgieva et al. (Int J Parasitol, 43:57-72, 2013). We detected ten cox 1 haplotypes among the isolates of D. spathaceum with only one haplotype shared with adult isolates from central and northern Europe. No specific geographic pattern of the distribution of the novel haplotypes was found.ConclusionThis first molecular exploration of the diversity of Diplostomum spp. in southern Europe indicates much lower species richness compared with the northern regions of Europe.

Effects of fishing on parasitism in a sparid fish: Contrasts between two areas of the Western Mediterranean

This study addressed the impacts of fishing on the rates of parasitism using the sparid Boops boops as a model fish species. Using a large suite of parasite species in B. boops, with different life histories, transmission pathways and host specificity, we compared parasite diversity, prevalence, abundance and community structure at two Mediterranean localities in the Balearic Sea, Santa Pola Bay and the Gulf of Oran, that are characterised by a contrasting pattern of fishing of B. boops. A total of 360 fish were examined comprising nine distinct samples collected during the warm and the cold weather months. A total of 29 parasite species were identified, with eight species in common for the two localities. Parasite component communities at Santa Pola Bay were more species rich and abundant than those at the Gulf of Oran and exhibited a different community structure. Of the eight common taxa used in the quantitative comparisons, five exhibited significant difference for prevalence between the two localities, four having substantially higher prevalence at Santa Pola and only one being more prevalent at the Gulf of Oran. Two specialist trematodes and the sparid generalist monogenean exhibited consistently higher prevalence and abundance at Santa Pola Bay than at the Gulf of Oran; the two specialists were also identified as key species for assigning individual fish to their locality of origin. The consistent differences in the richness, abundance and structure of parasite communities in B. boops from Santa Pola Bay and the Gulf of Oran may reflect the contrasting patterns of exploitation of the populations of this fish host at the two localities.

Abundance–variance and abundance–occupancy relationships in a marine host–parasite system: The importance of taxonomy and ecology of transmission

Abundance-occupancy and abundance-variance relationships are two of the most general macroecological patterns capturing essential fundamentals of the structuring of species distributions and are widely documented for free-living animal and plant species populations at different spatial scales. However, empirical data for parasites have been gathered using appropriate sampling designs only recently. We performed analyses across species of the variation in infection parameters and patterns of aggregation of the most widespread parasites in the marine sparid fish Boops boops across seven localities of two marine biogeographical regions, the North East Atlantic and the Mediterranean. We used a large dataset of multiple population samples replicated over time for 20 parasite species and carried out assessments both intraspecifically and interspecifically, across taxonomic and ecological groupings. This taxonomically diverse complex of species representing five major metazoan higher taxa with differing transmission ecologies allowed us to assess the effect of taxonomic and ecological determinants on the abundance-occupancy and abundance-variance relationships in the model marine host-parasite system. The results revealed that: (i) a power function, relating spatial variance to mean abundance, represents a suitable model for the spatial distribution of the species; (ii) prevalence, abundance and the degree of spatial heterogeneity are true species characteristics and differ consistently between higher level taxonomic groupings; (iii) infection parameters and abundance-variance relationship are dependent on host specificity and regional distribution patterns of the parasites; and (iv) the observed infection parameters agree well with predictions from the epidemiological negative binomial abundance-occupancy model built on parameters of Taylors power law both within and across species.

Follow-up trends of parasite community alteration in a marine fish after the Prestige oil-spill: shifting baselines?

This study evaluates the follow-up trends in the composition and structure of the parasite communities in the marine sparid Boops boops after the Prestige oil-spill. A total of 400 fish comprising 11 seasonal samples was analyzed from three impacted localities on the Atlantic coast of Spain. A large number of parasite species was recovered only after the spill thus suggesting a substantial alteration of the marine food webs. Post-spill communities exhibited higher richness and abundance due to the significant changes in the abundance of the common species, the latter indicating accelerated parasite transmission rates. Multivariate analyses at two nested scales detected a directional trend in parasite community succession towards the pre-spill situation, however, with no full support for community recovery. The state of parasite communities in 2005-2006 may provide the new baseline data which can serve as a framework for quantifying the impact of potential future spills in the region.

New molecular and morphological data for opecoelid digeneans in two Mediterranean sparid fishes with descriptions of Macvicaria gibsoni n. sp. and M. crassigula (Linton, 1910) (sensu stricto)

Molecular and morphological data were gathered for specimens of species of Macvicaria Gibson & Bray, 1982 and Pseudopycnadena Saad-Fares & Maillard, 1986 (Digenea: Opecoelidae) collected from two sparid fishes, Diplodus vulgaris (Geoffroy Saint-Hilaire) and Sparus aurata L., off the Algerian coast of the Western Mediterranean. Phylogenetic analyses based on ITS1-5.8S-ITS2 and partial 28S rDNA sequences provided evidence for the distinct species status of eight Mediterranean species of Macvicaria. Novel molecular data are provided for four species, M. gibsoni n. sp. and M. crassigula (Linton, 1910) (sensu stricto) based on specimens from D. vulgaris, and M. mormyri (Stossich, 1885) and M. maamouriae Antar, Georgieva, Gargouri & Kostadinova, 2015 based on specimens from S. aurata; descriptions of the molecular voucher material of the former three species are provided. Two species were delineated within the “crassigula” species complex of Macvicaria, M. gibsoni n. sp. and M. crassigula (s. str.), the distinctive differentiating features being the distribution of the dorsal vitelline fields in the forebody, confluent in M. gibsoni n. sp. and non-confluent in M. crassigula (s. str.), and the molecular data for both markers. Sequences associated with morphological description are also provided for the type-species of Pseudopycnadena, P. fischthali Saad-Fares & Maillard, 1986, based on material from D. vulgaris.

A new species of Bathycreadium Kabata, 1961 (Digenea: Opecoelidae) from Phycis blennoides (Brünnich) (Gadiformes: Phycidae) in the western Mediterranean.

Bathycreadium brayi n. sp. is described based on specimens collected from the deep-sea greater forkbeard Phycis blennoides (Brünnich) (Gadiformes: Phycidae) in the Western Mediterranean. The new species is distinguished from B. flexicolle Kabata, 1961, B. elongata (Maillard, 1970) and B. nanaflexicolle Dronen, Rubec & Underwood, 1977 by the much smaller size of the body and most organs, the large (in relation to body length and width) ventral sucker and the distinctly more anterior extent of the vitelline fields and from B. biscayense Bray, 1973 in having a narrower body, longer forebody and oesophagus, distinctly smaller ventral sucker and sucker width ratio and the shape of the gonads. Re-examination of the type-material of B. biscayense revealed that the original description of this species is based on composite material. A redescription of B. biscayense based on adult specimens from its type-host, Trachyrincus scabrus (Rafinesque), and new data based on the re-examination of the type-specimens of B. flexicolle and B. elongata are also provided.

Discrimination of fish populations using parasites: Random Forests on a ‘predictable’ host-parasite system

We address the effect of spatial scale and temporal variation on model generality when forming predictive models for fish assignment using a new data mining approach, Random Forests (RF), to variable biological markers (parasite community data). Models were implemented for a fish host-parasite system sampled along the Mediterranean and Atlantic coasts of Spain and were validated using independent datasets. We considered 2 basic classification problems in evaluating the importance of variations in parasite infracommunities for assignment of individual fish to their populations of origin: multiclass (2-5 population models, using 2 seasonal replicates from each of the populations) and 2-class task (using 4 seasonal replicates from 1 Atlantic and 1 Mediterranean population each). The main results are that (i) RF are well suited for multiclass population assignment using parasite communities in non-migratory fish; (ii) RF provide an efficient means for model cross-validation on the baseline data and this allows sample size limitations in parasite tag studies to be tackled effectively; (iii) the performance of RF is dependent on the complexity and spatial extent/configuration of the problem; and (iv) the development of predictive models is strongly influenced by seasonal change and this stresses the importance of both temporal replication and model validation in parasite tagging studies.

The Mediterranean: high discovery rates for a well-studied trematode fauna

Our knowledge of trematode diversity in Mediterranean Sea fishes is based on many contributions since the early 1800s (e.g. by Rudolphi, Stossich, Looss, Bartoli, Bray and Gibson). We have updated data from the Natural History Museum Host-Parasite Database and listed 302 digenean trematode species allocated to 146 genera in 29 families from 192 fish species (27% of the known fish-fauna) belonging to 76 families. The most diverse (with 31–41 species) digenean families (Opecoelidae Ozaki, 1925, Didymozoidae Monticelli, 1888 and Hemiuridae Looss, 1899) represent more than a third of the total richness (36% of species) and have been most frequently recorded (43% of the records). The overall mean number of species per host is close to recent global estimates for digenean richness in teleosts (1.57 vs 2.04, respectively), indicating a high diversity in the Mediterranean. The most diverse host families are also the best studied. However, three speciose host families (Rajidae de Blainville, Gobiidae Cuvier and Myctophidae Gill) appear under-studied and no digenean reports exist for 94 of 169 fish families present in the Mediterranean. Thus, although Mediterranean fishes appear well studied, further efforts are needed. Nevertheless, the descriptions of a large number of new taxa since 2000 indicate that focused efforts have resulted in a high discovery rate (2.4 species per year). Many of these new (often cryptic) taxa are the result of combined morphological and molecular methods, which promise more reliable estimates of digenean diversity in this region. We provide host-parasite lists for 192 species of fish in the Mediterranean comprising 890 host-parasite associations.

Metazoan parasite communities and diet of the velvet belly lantern shark Etmopterus spinax (Squaliformes: Etmopteridae): a comparison of two deep-sea ecosystems.

By combining an examination of stomach contents yielding a snapshot of the most recent trophic niche and the structure of parasite communities reflecting a long-term feeding niche, this study aimed at gaining more comprehensive information on the role of the small-sized deep-water velvet belly lantern shark Etmopterus spinax in the local food webs of the Galicia Bank and the canyon and valley system of the Avilés Canyon, which have been both proposed for inclusion in the Natura 2000 network of protected areas. As far as is known, this study provides the first comparative parasite infracommunity data for a deep-sea shark species. Component parasite communities in E. spinax were relatively rich, whereas the infracommunities were rather depauperate, with similar low diversity at both localities. The significant differences in the composition and structure of both parasite communities and prey assemblages indicate differential effects of the two deep-sea ecosystems on both long-term and most recent trophic niches of E. spinax. These results underline the importance of the use of multivariate analyses for the assessment of geographical variation in shark populations based on parasites and diet data.

An optimised multi-host trematode life cycle: fishery discards enhance trophic parasite transmission to scavenging birds ☆

Overlapping distributions of hosts and parasites are critical for successful completion of multi-host parasite life cycles and even small environmental changes can impact on the parasites presence in a host or habitat. The generalist Cardiocephaloides longicollis was used as a model for multi-host trematode life cycles in marine habitats. This parasite was studied to quantify parasite dispersion and transmission dynamics, effects of biological changes and anthropogenic impacts on life cycle completion. We compiled the largest host dataset to date, by analysing 3351 molluscs (24 species), 2108 fish (25 species) and 154 birds (17 species) and analysed the resultant data based on a number of statistical models. We uncovered extremely low host specificity at the second intermediate host level and a preference of the free-swimming larvae for predominantly demersal but also benthic fish. The accumulation of encysted larvae in the brain with increasing fish size demonstrates that parasite numbers level off in fish larger than 140mm, consistent with parasite-induced mortality at these levels. The highest infection rates were detected in host species and sizes representing the largest fraction of Mediterranean fishery discards (up to 67% of the total catch), which are frequently consumed by seabirds. Significantly higher parasite densities were found in areas with extensive fishing activity than in those with medium and low activity, and in fish from shallow lagoons than in fish from other coastal areas. For the first time, C. longicollis was also detected in farmed fish in netpens. Fishing generally drives declines in parasite abundance, however, our study suggests an enhanced transmission of generalist parasites such as C. longicollis, an effect that is further amplified by the parasites efficient host-finding mechanisms and its alteration of fish host behaviour by larvae encysted in the brain. The anthropogenic impact on the distribution of trophically-transmitted, highly prevalent parasites likely results in a strong effect on food web structure, thus making C. longicollis an ideal bioindicator to compare food webs in natural communities versus those impacted by fisheries and aquaculture.