A century of parasitology in fisheries and aquaculture.

Fish parasitological research associated with fisheries and aquaculture has expanded remarkably over the past century. The application of parasites as biological tags has been one of the fields in which fish parasitology has generated new insight into fish migration and stock assessments worldwide. It is a well-established discipline whose methodological issues are regularly reviewed and updated. Therefore, no concepts or case-studies will be repeated here; instead, we summarize some of the main recent findings and achievements of this methodology. These include the extension of its use in hosts other than bony fishes; the improvements in the selection of parasite tags; the recognition of the host traits affecting the use of parasite tags; and the increasingly recognized need for integrative, multidisciplinary studies combining parasites with classical methods and modern techniques, such as otolith microchemistry and genetics. Archaeological evidence points to the existence of parasitic problems associated with aquaculture activities more than a thousand years ago. However, the main surge of research within aquaculture parasitology occurred with the impressive development of aquaculture over the past century. Protozoan and metazoan parasites, causing disease in domesticated fish in confined environments, have attracted the interest of parasitologists and, due to their economic importance, funding was made available for basic and applied research. This has resulted in a profusion of basic knowledge about parasite biology, physiology, parasite-host interactions, life cycles and biochemistry. Due to the need for effective control methods, various solutions targeting host-parasite interactions (immune responses and host finding), genetics and pharmacological aspects have been in focus.

Genetic identification of Anisakis spp. (Nematoda: Anisakidae) from cetaceans of the Southwestern Atlantic Ocean: ecological and zoogeographical implications.

Adult Anisakis Dujardin, 1845 were found in two specimens of killer whale Orcinus orca and one specimen of franciscana Pontoporia blainvillei stranded from off the coast of Buenos Aires Province, Argentina. Genetic identification of the nematodes (N = 144) was performed by sequence analysis of the mitochondrial (mtDNA cox2) and the nuclear (nas 10 nDNA) gene loci. Anisakis pegreffii and Anisakis berlandi were detected in the two individuals of O. orca, while Anisakis typica and A. pegreffii were identified in P. blainvillei. Morphological and morphometric analysis also carried out on adult specimens of A. pegreffii and A. berlandi has allowed to underlining the usefulness of genetic/molecular markers in their recognition. This represents the first record of A. pegreffii in O. orca and P. blainvillei and of A. berlandi in O. orca. This is also the first sympatric and syntopic occurrence, as adults, of A. pegreffii and A. berlandi from the Austral Region of the Atlantic Ocean waters. These results provide insights into the knowledge of the host ranges and geographical distribution of these parasites in the basin waters of the region. Pontoporia blainvillei showed low abundance values of infection with Anisakis spp., which is the general pattern for coastal dolphins in the area, whereas O. orca harboured higher abundance of Anisakis spp. than those previously recorded among cetacean species in the Argentine Sea. Differences in the Anisakis spp. distribution and their parasitic loads, observed among the three host specimens, are discussed in relation to the oceanographic parameters, as well as to the host ecology. The usefulness of genetic/molecular markers in the recognition of adults of the sibling species A. pegreffii and A. berlandi with considerable overlapping in morphometric and morphological characters was underlined. The distribution of Anisakis species from Southwestern Atlantic waters is discussed in relation to their value as indicators for studies on the zoogeography of their hosts at a regional-scale level.

Profilicollis chasmagnathi (Acanthocephala) parasitizing freshwater fishes: paratenicity and an exception to the phylogenetic conservatism of the genus?

Polymorphid acanthocephalans are parasites of marine mammals, waterfowl and ichthyophagous birds. Among these, the genus Profilicollis is known to use exclusively decapods as intermediate hosts. Here, we report the first record of living cystacanths of Profilicollis parasitizing the body cavity of a fish host, Oligosarcus jenynsii, inhabiting the freshwater section of an estuarial system, Mar Chiquita coastal lagoon, in south-east Buenos Aires Province, Argentina. In this environment, cystacanths of Profilicollis chasmagnathi have been previously recorded infecting decapod crabs and as transient accidental infections in the gut of some carcinophagous fishes. In the present study, larvae from the crab Neohelice granulata, from the intestine of the estuarine fish Odontesthes argentinensis and from the body cavity of O. jenynsii were morphologically and genetically compared, confirming their identity as P. chasmagnathi, a species characteristic of estuaries and marine coasts along Argentina, Uruguay and Chile. These findings can be interpreted as a possible case of incipient paratenicity for Profilicollis, and a colonization event of freshwater habitats, probably promoted by the highly variable conditions, typical of ecotonal environments. In addition, cystacanths of the genus Polymorphus were also found in O. jenynsii, representing the first record of this genus in Oligosarcus from Argentina.

Are different parasite guilds of Pagrus pagrus equally suitable sources of information on host zoogeography?

Metazoan parasite assemblages of Pagrus pagrus inhabiting the southwestern Atlantic were analysed with the aim of identifying the existence of different stocks and to comparatively assess the value of different parasite guilds as indicators of zoogeographical regions. A total of 186 fish was examined. Samples were obtained from three Brazilian and one Argentine localities, distributed in three different biogeographic districts of the Argentine Zoogeographical Province. Pagrus pagrus harboured 26 metazoan parasite species distributed in three guilds, ectoparasites (10 species), long-lived larval endoparasites and short-lived gastrointestinal endoparasites (eight species each). Prevalence and abundance values of the former two guilds allowed analysing them comparatively to assess their value as biological indicators of both host population structure and zoogeography. Results of analyses on long-lived parasites evidenced the existence of three stocks, one in the regions of Rio de Janeiro and Sao Paulo, other in southern Brazil (Rio Grande do Sul) and a third in northern Argentina (Mar del Plata), responding to the differential environmental conditions characteristic of three zoogeographical ecoregions. Ectoparasite assemblages exhibited significant differences between all pairs of samples, including those considered as a single stock according to data on persistent parasites. Assemblages of long-lived larval parasites are considered as better indicators for stock assessment purposes than ectoparasites, whose population parameters were variable temporally and heterogeneous at small spatial scales. The distributional variability of persistent parasites of P. pagrus along large scales provides valuable information to help defining robust biogeographical patterns, applicable to stock identification and fishery management of this species.

Helminth parasites of South American fishes: current status and characterization as a model for studies of biodiversity.

The South American subcontinent supports one of the world's most diverse and commercially very important ichthyofauna. In this context, the study of South American fish parasites is of increased relevance in understanding their key roles in ecosystems, regulating the abundance or density of host populations, stabilizing food webs and structuring host communities. It is hard to estimate the number of fish parasites in South America. The number of fish species studied for parasites is still low (less than 10%), although the total number of host-parasite associations (HPAs) found in the present study was 3971. Monogeneans, with 835 species (1123 HPAs, 28.5%), and trematodes, with 662 species (1127 HPAs, 30.9%), are the more diverse groups. Data gathered from the literature are useful to roughly estimate species richness of helminths from South American fish, even though there are some associated problems: the reliability of information depends on accurate species identification; the lack of knowledge about life cycles; the increasing number of discoveries of cryptic species and the geographically biased number of studies. Therefore, the closest true estimations of species diversity and distribution will rely on further studies combining both molecular and morphological approaches with ecological data such as host specificity, geographical distribution and life-cycle data. Research on biodiversity of fish parasites in South America is influenced by problems such as funding, taxonomic impediments and dispersion of research groups. Increasing collaboration, interchange and research networks in the context of globalization will enable a promising future for fish parasitology in South America.

Assessing the role of host traits as drivers of the abundance of long-lived parasites in fish-stock assessment studies.

In order to identify the best tools for stock assessment studies using fish parasites as biological indicators, different host traits (size, mass and age and their interaction with sex) were evaluated as descriptors of cumulative patterns of both parasite abundance and infracommunity species richness. The effect of such variables was analysed for a sample of 265 specimens of Percophis brasiliensis caught in the Argentine Sea. The abundances and species richness were modelled using generalized linear mixed models (GLMMs) with negative binomial and Poisson distribution respectively. Due to collinearity, separate models were fitted for each of the three main explanatory variables (length, mass and age) to identify the optimal set of factors determining the parasite burdens. Optimal GLMMs were selected on the basis of the lowest Akaike information criteria, residual information and simulation studies based on 10 000 iterations. Results indicated that the covariates length and sex consistently appeared in the most parsimonious models suggesting that fish length seems to be a slightly better predictor than age or mass. The biological causes of these patterns are discussed. It is recommended to use fish length as a measure of growth and to restrict comparisons with fish of similar length or to incorporate length as covariate when comparing parasite burdens. Host sex should be also taken into account for those species sexually dimorphic in terms of morphology, behaviour or growth rates.

Myxozoans as biological tags for stock identification of the Argentine hake, Merluccius hubbsi (Gadiformes: Merlucciidae).

Myxozoans have been successfully used as tags for fish stock identification around the world. However, few studies using myxozoan tags have been carried out in the Southern Atlantic, a region with complex oceanography that constitutes a potentially suitable scenario for testing the utility of myxozoans as indicators. Its usefulness was tested using six samples of Merluccius hubbsi in two different regions of the Argentine Sea. Generalized linear models were performed to assess the effects of fish size and sex, and year and region of capture and selected using the Information Theoretic approach. Three myxozoan species were recorded: Kudoa rosenbuschi, Myxoproteus meridionalis and Fabespora sp. Results of modelling species individually showed differential capabilities for detecting geographical population structure at different spatial scales, with K. rosenbuschi and Fabespora sp. allowing the discrimination of northern and southern stocks, but Fabespora sp. also as a promissory indicator of intrapopulation sub-structure due to different migratory routes during non-reproductive periods. This work confirms that myxozoans offer a set of suitable markers at different spatial scales, which can be selected individually or in any combination, depending on the geographical extent of the study, constituting tools adaptable to the objectives of further research on fish population structure.

Homogeneity of parasite assemblages of Dules auriga (Serranidae) in hydrographically heterogeneous sites.

Parasite assemblages of Dules auriga are described for the first time from samples caught during research cruises in two localities of the Argentine-Uruguayan Common Fishing Zone (AUCFZ) and are compared with four additional samples collected by commercial catches from the same region. A total of 178 fish were examined and 13 parasite species were found. This showed low species richness, a condition observed in some other small benthic species at a low trophic level. The composition of the parasite fauna was similar to those found on other host species in the region, sharing the same set of dominant species with other sympatric fishes, which have been identified as both typical and as indicators of this ecoregion: Grillotia carvajalregorum, Corynosoma australe and Hysterothylacium sp. Multivariate similarity analyses at the infracommunity and the component community levels indicated that the two samples caught at different latitudes in the AUCFZ display almost identical parasite assemblages. This repeatability in assemblage structure was also observed across samples from commercial catches. The homogeneity of the parasite assemblages is considered to be an intrinsic property of fish inhabiting the AUCFZ, independent of their ecology and trophic level.

Marine parasites as biological tags in South American Atlantic waters, current status and perspectives.

Many marine fisheries in South American Atlantic coasts (SAAC) are threatened by overfishing and under serious risk of collapsing. The SAAC comprises a diversity of environments, possesses a complex oceanography and harbours a vast biodiversity that provide an enormous potential for using parasites as biological tags for fish stock delineation, a prerequisite for the implementation of control and management plans. Here, their use in the SAAC is reviewed. Main evidence is derived from northern Argentine waters, where fish parasite assemblages are dominated by larval helminth species that share a low specificity, long persistence and trophic transmission, parasitizing almost indiscriminately all available fish species. The advantages and constraints of such a combination of characteristics are analysed and recommendations are given for future research. Shifting the focus from fish/parasite populations to communities allows expanding the concept of biological tags from local to regional scales, providing essential information to delineate ecosystem boundaries for host communities. This new concept arose as a powerful tool to help the implementation of ecosystem-based approaches to fisheries management, the new paradigm for fisheries science. Holistic approaches, including parasites as biological tags for stock delineation will render valuable information to help insure fisheries and marine ecosystems against further depletion and collapse.

Stocks and seasonal migrations of the flounder Xystreurys rasile as indicated by its parasites.

The aims of this study were (1) to compare the structure and composition of parasite assemblages of the flounder Xystreurys rasile in two regions of the Argentine Sea in order to evaluate the hypothesis for the existence of different stocks, and (2) to test the hypothesis for X. rasile migration from the Argentine-Uruguayan Common Fishing Zone (AUCFZ) towards more southern waters during spring. Parasitological evidence shows that at least two stocks of X. rasile inhabit the coastal and shelf waters of the northern Argentine Sea, one in El Rincón and the other in the AUCFZ. These stocks should be considered as discrete entities in management plans to ensure a sustainable use of these resources. The results also confirm the existence of migratory patterns in the northern stock.

Ontogenetic changes in heterogeneity of parasite communities of fish: disentangling the relative role of compositional versus abundance variability.

In order to determine how much of the variability in parasite assemblages is driven by differences in composition or in abundance we used multivariate dispersions (average distance from infracommunities to their size class centroid in the multivariate space) as a measurement of ß-diversity in infracommunities of Conger orbignianus, applying a set of dissimilarity measures with different degrees of emphasis on composition versus relative abundance information. To evaluate comparatively the rate of such changes, we also analysed the effect of host size by regressing differences in ß-diversity among size classes against differences in mean fish size. Multivariate dispersions varied along an ontogenetic gradient, its significance depending on the measurement used. Larger fish showed higher richness and abundance; however, smaller fish displayed lower variations in abundance but higher in composition. This could be caused by stochastic encounters at low densities due to the overdispersion of parasites in previous hosts. As fish grow, the composition of their parasite assemblages becomes homogenized by repeated exposure, with abundance thus arising as the main source of variability. Both variables act at different rates, with the exponential decay in the compositional variability as differences in fish size increase being about twice as steep as the decay in abundance variability, indicating that compositional homogeneity is reached faster than abundance heterogeneity as fish grow. Discerning between both variables is crucial in order to understand how community structure is formed by size-dependent variability of host populations.

Similarity in parasite community structure may be used to trace latitudinal migrations of Odontesthes smitti along Argentinean coasts.

The aims of this study were to determine the existence of migratory movements and to identify ecological stocks of the silverside Odontesthes smitti along its distribution in the Southern Atlantic Ocean, using metazoan parasites as biological tags. Samples were obtained from San José Gulf (SJ) (42° 25' S; 64° 07' W) and Nuevo Gulf (NG) (42° 47' S; 65° 02' W) in north Patagonia during winter and summer and in waters off Mar del Plata (MDP) (38° 03' S; 57° 32' W), Bonaerense region, during winter. Fifteen parasite species were collected. Multivariate statistical procedures on parasite community data showed strong effect of host size on the structure of parasite assemblages. Taking into account the variations among samples due to host size, the differential structure of parasite communities between SJ and NG suggests that fish inhabiting these localities could belong to different ecological stocks. Fish from MDP and SJ caught in summer showed similar composition in their parasite assemblages, which is congruent with a migratory cycle that implies that fish caught in MDP during winter inhabit SJ during summer. Further evidence of the Patagonian origin of MDP O. smitti is the presence of the digenean Proctotrema bartolii in fish from both regions. Proctotrema bartolii is acquired by O. smitti only in the Magellanic province, where its intermediate host, Darina solenoides, is distributed. The analyses suggest that O. smitti inhabiting north Patagonian gulfs could belong to different ecological stocks and that O. smitti caught in MDP could have come from SJ.

Fish trophic level and the similarity of non-specific larval parasite assemblages.

Whereas the effect of parasites on food webs is increasingly recognised and has been extensively measured and modelled, the effect of food webs on the structure of parasite assemblages has not been quantified in a similar way. Here, we apply the concept of decay in community similarity with increasing distance, previously used for parasites in geographical, phylogenetic and ontogenetic contexts, to differences in the trophic level (TL) based on diet composition of fishes. It is proposed as an accurate quantitative method to measure rates of assemblage change as a function of host feeding habits and is applied, to our knowledge for the first time, across host species in marine waters. We focused on a suite of 15 species of trophically-transmitted and non-specific larval helminths across 16 fish species (1783 specimens, six orders, 14 families) with different sizes and TLs, gathered from the same ecosystem. Not all host species harboured the same number and types of parasites, reflecting the differences in their ecological characteristics. Using differences in TL and body length as measurements of size and trophic distances, we found that similarity at both infracommunity and component community levels showed a very clear decay pattern, based on parasite abundance and relative abundance, with increasing distance in TL, but was not related to changes in fish size, with TL thus emerging as the main explanatory factor for similarity of parasite assemblages. Furthermore, the relationships between host TL and assemblage similarity allowed identification of fishes for which the TL was under- or over-estimated and prediction of the TL of host species based on parasite data alone.

Parasitism underground: determinants of helminth infections in two species of subterranean rodents (Octodontidae).

Patterns of infection among hosts in a population are often driven by intrinsic host features such as age or sex, as well as by positive or negative interactions between parasite species. We investigated helminth parasitism in 2 South American rodent species, Ctenomys australis and C. talarum (Octodontidae), to determine whether the unusual solitary and subterranean nature of these hosts would impact their patterns of infection. We applied generalized linear models to infection data on a total of 7 helminth species (1 in C. australis and 6 in C. talarum). Host age and season of capture influenced infection levels in some of the helminth species, but none were influenced by host body condition. In C. talarum, 4 pairs of helminth species showed significant associations, either asymmetrical or symmetrical, and with 3 of the 4 being positive; strong inter-specific facilitation appears likely in 1 case. Also, we found that female hosts, especially non-pregnant ones, harboured heavier infections of 2 nematode species than male hosts. This is in sharp contrast to the general male-bias reported for most studies of nematodes in wild mammals, and we develop explanations for these results based on the unusual ecology of these subterranean rodents.

Consequences of microhabitat selection for reproductive success in the parasitic copepod Neobrachiella spinicephala (Lernaeopodidae).

SUMMARY: Narrow site specificity in parasites is assumed to be associated with fitness benefits, such as higher reproductive success, although this is never quantified. We linked the body mass and combined mass of egg sacs of female copepods, Neobrachiella spinicephala, parasitic on the sandperch, Pinguipes brasilianus, to attachment sites on the host. Adult females attach permanently either on the lips, the margins of the operculum, or the base of pectoral or pelvic fins. In addition to influences of sampling site, season and host body length, our analyses revealed important fitness effects. First, attachment site significantly influenced copepod body mass; independent of other factors, copepods at the base of fins were 32% larger than those on the lips or operculum. Second, the mass of egg sacs was almost always greater if the copepod was attached at the base of fins rather than to the lip or operculum. Thus, a female weighing 6 mg would, on average, produce 40% larger egg sacs if attached to the base of fins. However, copepods were much more likely to attach at the base of fins on small fish, and on either the lip or the operculum on large fish. We propose that constraints varying with fish size account for the shift from optimal to suboptimal attachment sites as a function of increasing host size. By measuring differences in fitness components between attachment sites, our approach allows hypothesis testing regarding microhabitat selection.

The metazoan parasite communities of the Argentinean sandperch Pseudopercis semifasciata (Pisces: Perciformes) and their use to elucidate the stock structure of the host.

The use of parasites as biological tags allowed the identification of 3 stocks of Argentinean sandperch, Pseudopercis semifasciata (Cuvier), in the Argentine Sea. A total of 100 specimens caught in 3 zones: Villa Gesell (37 degrees 15'S, 57 degrees 23'W; n=20), Miramar (38 degrees 03'S, 57 degrees 30'W-38 degrees 44'S, 58 degrees 44'W; n=30) and Península Valdes (42 degrees 00'-42 degrees 45'S; n=50), were examined and 28 parasite species were found, 15 of them being new host records. Both univariate and multivariate analyses identified discrete stocks in each zone. The observed differences were not related to the host size or sex. Each locality was characterized by its own indicator species. Villa Gesell was typified by unidentified cestode plerocercoids, Corynosoma cetaceum and Hysterothylacium sp., Miramar by Heterosentis sp. and Pseudoterranova sp. and Península Valdes by A. simplex s.l. Fishes from both northern localities shared gnathiid pranizae, Corynosoma australe and Grillotia sp. as indicators, whereas Miramar and Península Valdes shared only Trifur tortuosus. The most distant localities showed no indicator species in common. Discriminant analyses of parasite assemblages agreed with populational comparisons in identifying the same set of biological tags, whereas some differences in the identity of indicator species were obtained by similarity analysis. However, the 3 approaches were congruent in identifying Grillotia sp., C. australe and C. cetaceum as indicators of northern localities, and A. simplex s.l. as related to Patagonian waters. Differences among zones could be enhanced by the sedentary habits, limited dispersal and high site fidelity of P. semifasciata, and their spawning in rocky outcrops, which are isolated environments.

Parasite infracommunities of a specialized marine fish species in a compound community dominated by generalist parasites.

The structure and composition of parasite communities of Mullus argentinae were analysed under two alternative hypotheses in a sample of 75 specimens caught off Mar del Plata, Argentina (38 degrees 27'S, 57 degrees 90'W). The first, based on the dominance of trophically transmitted larval parasites of low host-specificity among fish species in the region, predicts that infracommunities will be random subsets of regionally available species. The second, based on previous studies on other mullids, predicts that infracommunities will be dominated by adult digeneans. The parasite fauna of goatfishes was mainly composed of endoparasites, with metacercariae of Prosorhynchus australis accounting for most individual parasites and greatly affecting infracommunity descriptors. Its importance was reinforced by the low number of trophically transmitted larval parasites. Both hypotheses were refuted; parasite communities were not dominated either by trophically transmitted larval parasites of low host-specificity or by adult digeneans. Prosorhynchus australis was the only species displaying any degree of phylogenetic specificity. Therefore, the influence of phylogenetic factors seems to exceed that of ecological ones in determining the observed structure of infracommunities. However, it is precisely host ecology that allows P. australis to become the determinant of infracommunity structure by constraining the acquisition of other parasites. Studies aiming to determine the relative importance of evolutionary and ecological processes as structuring forces of parasite communities should take into account not only the identity and specificity of their component parasites, but also their availability in the compound community.

Seasonal stability and spatial variability of parasites in Brazilian sandperch Pinguipes brasilianus from the Northern Argentine Sea: evidence for stock discrimination.

The use of parasites as biological tags allowed the identification of two stocks of Brazilian sandperch Pinguipes brasilianus, in the Bonaerense region of the Argentine Sea. A total of 156 adult specimens of P. brasilianus were examined for parasites. Temporal variability in parasite burdens was assessed from fish caught seasonally in coastal waters of two zones, south Bonaerense (during autumn and winter) and north Bonaerense (during summer). Additional data from a previous study, comprising P. brasilianus caught during spring in these two zones, as well as in two populations from north Patagonian gulfs were used for comparative analyses of spatial variability. A total of 14 193 metazoan parasites belonging to 19 species were found. Comparisons of seasonal variability in pooled samples and within each locality showed that locality effects exceeded seasonal ones, suggesting the possible existence of two discrete stocks in the Bonaerense region. These findings were strongly supported by discriminant analyses and comparisons of prevalence and abundance between zones, after pooling seasonal samples within each zone. Further evidence of the discreteness of both stocks was assessed by inclusion of samples from Patagonian gulfs in the discriminant analysis, confirming that their differences were at a inter-population level. The parasite species that contributed most to the separation of the samples were generally those identified as biological markers in previous studies. Differing oceanographic conditions are discussed as potential causes of inter-population variation of parasite burdens.

Genetic relationships among species of Contracaecum Railliet & Henry, 1912 and Phocascaris Höst, 1932 (Nematoda: Anisakidae) from pinnipeds inferred from mitochondrial cox2 sequences, and congruence with allozyme data.

The genetic relationships among 11 taxa, belonging to the genus Contracaecum (C. osculatum A, C. osculatum B, C. osculatum (s.s.), C. osculatum D, C. osculatum E, C. osculatum baicalensis, C. mirounga, C. radiatum, C. ogmorhini (s.s.), C. margolisi) and Phocascoris (Phocoscris cystophorae), parasites as adults of seals, were inferred from sequence analysis 1519 bp) of the mitochondrial cytochrome c oxidase subunit II (mtDNA cox2) gene. Phylogenetic analyses obtained from Parsimony (MP) and Neighbour-Joining (NJ) K2P distance values generated similar topologies, each well supported at major nodes. All analyses delineated two main clades: the first encompassing the parasites of the phocid seals, i.e. the C. osculatum species complex, C. osculatum boicolensis, C. mirounga and C. radiatum, with the latter two species forming a separate subclade; the second including the parasites of otarids, i.e. C. ogmorhini (s.s.) and C. margolisi. An overall high congruence between mtDNA inferred tree topologies and those produced from nuclear data sets (20 allozyme loci) was observed. Comparison of the phylogenetic hypothesis here produced for Controcaecum spp. plus Phocascaris with those currently available for their definitive hosts (pinnipeds) suggests parallelism between hosts and parasite phylogenetic tree topologies.