Fish population studies using parasites from the Southeastern Pacific Ocean: considering host population changes and species body size as sources of variability of parasite communities.

Research using parasites in fish population studies in the South Eastern Pacific (SEP) is summarized. There are 27 such studies (snapshots mainly) in single host species sampled at different geographic localities and at somewhat similar times. They have been devoted mainly to economically important species, though others on coastal and intertidal fish or on less- or non-commercial species provide insights on scales of temporal and spatial variation of parasite infracommunities. Later, we assess whether the probability of harbouring parasites depends on the host species body size. Our results indicate that a stronger tool for fish population studies may be developed under regular (long term) scrutiny of parasite communities, especially of small fish host species, due to their larger variability in richness, abundance and total biomass, than in large fish species. Finally, it might also be necessary to consider the effects of fishing on parasite communities as well as the natural oscillations (coupled or not) of host and parasite populations.

Parasites of fish larvae: do they follow metabolic energetic laws?

Eumetazoan parasites in fish larvae normally exhibit large body sizes relative to their hosts. This observation raises a question about the potential effects that parasites might have on small fish. We indirectly evaluated this question using energetic metabolic laws based on body volume and the parasite densities. We compared the biovolume as well as the numeric and volumetric densities of parasites over the host body volume of larval and juvenile-adult fish and the average of these parasitological descriptors for castrator parasites and the parasites found in the fish studied here. We collected 5266 fish larvae using nearshore zooplankton sampling and 1556 juveniles and adult fish from intertidal rocky pools in central Chile. We considered only the parasitized hosts: 482 fish larvae and 629 juvenile-adult fish. We obtained 31 fish species; 14 species were in both plankton and intertidal zones. Fish larvae exhibited a significantly smaller biovolume but larger numeric and volumetric densities of parasites than juvenile-adult fish. Therefore, fish larvae showed a large proportion of parasite biovolume per unit of body host (cm(3)). However, the general scaling of parasitological descriptors and host body volume were similar between larvae and juvenile-adult fish. The ratio between the biovolume of parasites and the host body volume in fish larvae was similar to the proportion observed in castrator parasites. Furthermore, the ratios were different from those of juvenile-adult fish, which suggests that the presence of parasites implies a high energetic cost for fish larvae that would diminish the fitness of these small hosts.

First report of a member of the family Mermithidae parasitizing the sandhopper Orchestoidea tuberculata (Amphipoda, Talitridae) in Chile.

Specimens of the sandhopper Orchestoidea tuberculata (Amphipoda; Talitridae) collected from sandy beaches in south-central Chile, were found to be parasitized by juvenile mermithids, constituting the first record of a mermithid infecting a marine amphipod in Chile. A morphological description of juveniles is provided. Sequence analyses based on mitochondrial COI and nuclear 18S rDNA of the mermithids showed extremely low genetic variation. Phylogenetic analyses indicate that the mermithid is more closely related to Hexamermis agrotis, which parasitize Coleoptera, than to Thaumamermis zealandica, which parasitizes New Zealand confamilial talitrid amphipods.

Effects of the cranial parasite Tylodelphys sp. on the behavior and physiology of puye Galaxias maculatus (Jenyns, 1842).

Diplostomatid digeneans are well-known manipulators of the behavior of their intermediate hosts. Unencysted metacercariae of Tylodelphys sp. inhabit the cranial cavity of the fish Galaxias maculatus; however, to date they have not been documented to alter their host behavior. The goal of this study was to evaluate the potential effects of Tylodelphys sp. inhabiting the cranial cavity of Galaxias maculatus on host physiology and swimming behavior as well as its reaction to a simulated predation attempt. Blind experiments in the lab were carried out on 56 fish that were filmed individually. The Fulton condition factor (K) was used as an approximation of nutritional status and a respirometry chamber was used to evaluate oxygen consumption rates of fish. Of the 56 fish, 21 were parasitized by Tylodelphys sp. (mean intensity = 30, range from 1 to 101). Parasitized and non-parasitized fish were similar in condition factor and oxygen consumption rates. Furthermore, the oxygen consumption rate of G. maculatus was not correlated with the abundance of Tylodelphys sp. However, parasitized fish more frequently swam close to the water surface, whereas non-parasitized fish more frequently swam at intermediate depths. When faced with a simulated predator attack, unparasitized fish showed more frequent fleeing behavior as well as a more intense post-fleeing activity. Collectively, these results suggest that Tylodelphys sp. inhabiting the cranial cavity of fish may alter their behavior predisposing them to predation by birds.

GEOGRAPHICAL VARIATION OF ENTEROPARASITISM IN THE SOUTHERN SEA LION OTARIA FLAVESCENS (SHAW, 1800) OFF THE COAST OF CHILE AS EVIDENCED WITH COPROLOGICAL TESTS: IMPLICATONS FOR ZOONOTIC RISKS.

The scarce information on the helminth fauna in otariids from the Southeastern Pacific comes mainly from stranded individuals or killed for that purpose. In this study, we compared the abundance and composition of enteroparasitic assemblages of Otaria flavescens using coprological techniques. Three sampling localities from north to south spanning 2,200 km off the Chilean coast were considered (Iquique, Viña del Mar, and Talcahuano). In all, 60 fecal samples were collected, and eggs belonging to 5 taxa were found in 91.6% of the samples. They were the anisakid nematodes Contracaecum and Pseudoterranova, the cestode Adenocephalus (syn. Diphyllobothrium), the trematode Ogmogaster, and the acanthocephalan Corynosoma. Samples from southern Chile (Talcahuano) showed the highest prevalence. Adenocephalus eggs had the highest prevalence and abundance in Iquique and Talcahuano, whereas Ogmogaster was the less prevalent and abundant in all sampling localities. Corynosoma eggs had similar prevalence and abundance among sampling localities, and Pseudoterranova eggs were absent in Iquique and with median prevalence values in Viña del Mar and Talcahuano. Thus, the composition of parasite egg assemblages was different between sampling localities. These differences between sampling localities may help to explain differential records of some zoonotic parasitoses such as pseudoterranovosis and diphyllobothriosis in Peru and Chile, where consumption of raw or marinated fish (ceviche) is common. For example, the lower diversity of parasite egg assemblages in the northern Chilean coast may be due to the absence or lower abundance of first intermediate/paratenic hosts of Pseudoterranova.

Molecular and experimental evidence refuse the life cycle of Proctoeces lintoni (Fellodistomidae) in Chile.

The mussel Perumitylus purpuratus has been described as the first intermediate host for the digenea Proctoeces lintoni (Fellodistomidae) in the Chilean coast. The study of more than 3000 specimens of P. purpuratus, taken off northern Chile revealed the absence of sporocysts. Experimental infection of mussels with eggs obtained from the known host for P. lintoni was unsuccessful. We analyze the V4 region of the SSU rRNA of living sporocysts and cercariae obtained from P. purpuratus from central Chile in order to confirm the proposed life cycle for this digenea. Our results demonstrated that sporocysts and cercariae obtained from P. purpuratus do not belong to P. lintoni but to an undescribed digenea from the Chilean coast.

Helminth Community Structure of the Gray Four-Eyed Opossum Philander opossum (Mammalia: Didelphidae) in the Neotropical Portion of Mexico.

Studies on helminth communities associated with didelphids are scarce; the majority of works have focused at taxonomic level. To increase the ecological knowledge of these host-parasite associations, during March (dry season) of 3 consecutive years (2013-2015) a total of 49 adults of the gray four-eyed opossum (Philander opossum) was collected in the Neotropical portion of Mexico (Agua Fría, Chiapas State) and examined for helminths. The main objectives of this study were to describe the infra- and component communities of helminths associated with P. opossum and to compare the helminth fauna of the Mexican population of this host species with those studied in French Guiana and in other Mexican terrestrial didelphids. The helminthological record of this host consisted of 12 species: 7 taxa of Nematoda, 3 of Trematoda, 1 Cestoda, and 1 Acanthocephala. Eight of the 12 taxa have been previously recorded in Didelphidae and 4 represent accidental infections ( Glossocercus sp., Stomylotrema vicarium, Spirura mexicana and Acanthocephala gen. sp.). Diet of hosts is the main structuring factor of the communities (92% of the helminth species were recruited through ingestion). Forty-eight hosts were parasitized by at least 1 helminth species; Rhopalias coronatus was the most prevalent and abundant species in the hosts sampled. No significant differences were found in global prevalence among the helminth species present in all samplings, considering host sex and year. The dominance exerted by R. coronatus led to low values of evenness and diversity at both community levels. No significant differences were observed in composition of helminth species among the 3 sampling years regarding sex. The results of our study showed changes in helminth abundance at infracommunity level; during the first sampling these changes are explained by species with direct life cycle ( Viannaia sp. and Cruzia tentaculata), whereas in last 2 surveys the explanation can be attributed to species with heteroxenous life cycles (particularly R. coronatus, Duboisiella proloba, and Turgida turgida). Thirty-three percent of the helminth species recorded in P. opossum in Agua Fría is shared with the other 2 terrestrial species of didelphids sampled in different sites of Mexico: Didelphis marsupialis and Didelphis virginiana. In contrast, samples from French Guiana and Agua Fría, differ in terms of helminth fauna, confirming that the helminth communities of opossum species inhabiting the same locality show higher levels of taxonomic similarity than communities of conspecific marsupials allopatrically distributed.

A new species of Proctoeces and reinstatement of Proctoeces humboldti George-Nascimento and Quiroga 1983 (Digenea: Fellodistomidae) based on molecular and morphological evidence.

The most studied digenean of marine organisms in Chile is by far Proctoeces humboldti, a parasite of the intestine of the clingfish Sicyases sanguineus and gonad of the keyhole limpet Fissurella spp. (progenetic metacercariae). The mussel Perumytilus purpuratus has been suggested as the first intermediate host for this digenean. In a study examining the parasites of S. sanguineus from central Chile, we found specimens of Proctoeces showing significant morphological differences with P. humboldti. To assist in the resolution of the taxonomic identification of these specimens, as well sporocysts obtained from the mussel P. purpuratus from central and northern Chile, phylogenetic studies using DNA sequences from the SSU rRNA, as well the LSU rRNA and Cox 1 gene were performed. Results showed that the clingfish S. sanguineus is a host for two species of Proctoeces (P. humboldti and P. syciases n. sp.) along the northern and central Chilean coast, without geographic separation; the mussel P. purpuratus is the first intermediate host for P. syciases n. sp. but not for P. humboldti in central and northern Chile. Fissurellids (Archaeogastropoda) along the Chilean coast harbor only progenetic stages of P. humboldti, but there is no evidence of progenesis for P. syciases. The reinstatement of Proctoeces humboldti is strongly suggested.

The scaling of total parasite biomass with host body mass.

The selective pressure exerted by parasites on their hosts will to a large extent be influenced by the abundance or biomass of parasites supported by the hosts. Predicting how much parasite biomass can be supported by host individuals or populations should be straightforward: ultimately, parasite biomass must be controlled by resource supply, which is a direct function of host metabolism. Using comparative data sets on the biomass of metazoan parasites in vertebrate hosts, we determined how parasite biomass scales with host body mass. If the rate at which host resources are converted into parasite biomass is the same as that at which host resources are channelled toward host growth, then on a log-log plot parasite biomass should increase with host mass with a slope of 0.75 when corrected for operating temperature. Average parasite biomass per host scaled with host body mass at a lower rate than expected (across 131 vertebrate species, slope=0.54); this was true independently of phylogenetic influences and also within the major vertebrate groups separately. Since most host individuals in a population harbour a parasite load well below that allowed by their metabolic rate, because of the stochastic nature of infection, it is maximum parasite biomass, and not average biomass, that is predicted to scale with metabolic rate among host species. We found that maximum parasite biomass scaled isometrically (i.e., slope=1) with host body mass. Thus, larger host species can potentially support the same parasite biomass per gram of host tissues as small host species. The relationship found between maximum parasite biomass and host body mass, with its slope greater than 0.75, suggests that parasites are not like host tissues: they are able to appropriate more host resources than expected from metabolically derived host growth rates.

Two new species of Ascarophis (Nematoda: Cystidicolidae) in marine fishes from Chile.

In this study, we describe 2 new species of Ascarophis van Beneden, 1871 (Nematoda: Cystidicolidae), found in fishes from southern Chile. Ascarophis carvajali n. sp. was found in Austrolycus depressiceps and Patagonotothen cornucola, whereas Ascarophis draconi n. sp. was taken from Champsocephalus gunnari. These new Ascarophis species differ from other species in a combination of several morphometric and morphological characteristics. Although A. carvajali n. sp. was morphologically close to Ascarophis minuta, the new species has a larger ratio between glandular and muscular esophagus, filaments on both egg poles, and a shorter right spicule than A. minuta. Ascarophis draconi n. sp. was morphologically similar to Ascarophis adioryx and Ascarophisfiliformis. However, A. adioryx has eggs without filaments, a smaller ratio between glandular and muscular esophagus length, and a smaller ratio between left and right spicule lengths in contrast to A. draconi n. sp., whereas A. filiformis has a shorter glandular esophagus and left spicule length than A. draconi n. sp. Only 1 Ascarophis species has been recorded in a single fish from Chile (i.e., Ascarophis sebastodis in Sebastes capensis). Consequently, this study constitutes not only new species and records of Ascarophis in fishes from Chile, but also new records for the Pacific coast of South America.

Dispersal of Udonella australis (Monogenea: Udonellidae) between caligid copepods Caligus rogercresseyi and Lepeophtheirus mugiloidis on Chilean rock cod.

Udonella australis is a platyhelminth that lives on the surface of the ectoparasite copepods Caligus rogercresseyi and Lepeophtheirus mugiloidis, which coexist on the Chilean rock cod Eleginops maclovinus. The absence of a planktonic oncomiracidium stage in the life cycle of udonellids may limit their dispersal ability. However, the high prevalence and intensity of U. australis on C. rogercresseyi suggest they have developed dispersal strategies to compensate for the lack of a free-living larval stage. The goals of this study were to determine the main dispersal mechanisms of U. australis in 1 copepod species and to compare the dispersal ability of U. australis between 2 different copepod species. Chilean rock cods were infected with female (without udonellids) and male (with and without udonellids) C. rogercresseyi. Other fishes were also infected with this copepod (with U. australis) and with L. mugiloidis (without U. australis). The dispersal of udonellids among copepods occurs through both intraspecific and interspecific processes. The main dispersal mechanism appears to be copepod mating; contact between same-sex individuals is less important. Intraspecific dispersal seems to be more dependent on the number of udonellids per fish than on copepod abundance, as observed for interspecific dispersal.

Two new species of digeneans (Lecithasteridae and Haploporidae) of the intertidal blenny Scartichthys viridis (Valenciennes) from the central coast of Chile.

Two new digenean species are described from the intertidal blenny Scartichthys viridis (Valenciennes) (Blenniidae) collected off the coasts of Chile. The digenean Monorchimacradena viridis n. sp. (Lecithasteridae: Macradenininae) differs from the only known species described in the genus, M. acanthuri Nahhas and Cable 1964, in the presence of Drüsenmagen in the caeca, the location of the seminal vesicle between the testis and ovary (anterior to the testis in M. viridis n. sp.), and the pre-ovarian vitellarium. Megasolena littoralis n. sp. (Haploporidae), which is also reported from Scartichthys gigas (Steindachner), differs from the five valid species of Megasolena in that the post-caecal region (from the posterior edge of the caeca to the end of the body) is larger in M. viridis n. sp., meaning that the caeca are shortest in this species. Also, M. littoralis n. sp. is distinguished, from the other congeneric species, in a combination of characteristics, e.g., body length, suckers, pharynx, testes, hermaphroditic sac and sucker-length ratio. Sequences of ITS2 rDNA were generated for specimens of both species from various localities, indicating that it was invariant within the species. This study describes species of Monorchimacradena and Megasolena in Chilean waters, here reported for the first time off the Pacific Coast of South America.

A new species of Hemipera Nicoll, 1913 (Digenea: Derogenidae) from fishes of the intertidal rocky zone of Chile.

A new species, Hemipera cribbi sp. nov., is described. This trematode was found in three intertidal fish species: Scartichthys viridis (Valenciennes) (Blenniidae), Gobiesox marmoratus Jenyns (Gobiesocidae) and Myxodes viridis Valenciennes (Clinidae) from the central and southern coast of Chile. Of 233 individuals of S. viridis from the central coast examined, 19 were infected. From the southern coast, nine individuals of S. viridis (one infected), five individuals of G. marmoratus (four infected), and 16 individuals of M. viridis (one fish infected) were examined. Hemipera cribbi sp. nov. is distinguished from the five other congeneric species mainly in the body size, being the smallest and narrowest species in the genus, reaching five times longer than wide. This is the first species of the genus described for the South Pacific Ocean off South America. ITS2 rDNA sequences of Hemipera cribbi sp. nov. from each host and locality were identified.

Spiracanthus bovichthys n. gen. n. sp. (Acanthocephala: Arhythmacanthidae), a parasite of littoral fishes of the central south coast of Chile.

A new acanthocephalan species, Spiracanthus bovichthys n. gen. n. sp., is described. Samples were taken from 26 marine fish species between 23 and 53 degrees S of Chile. The parasite was found in the intestine of 6 species and only between 36 and 40 degrees S, especially in those fish that prey on small crustaceans in the upper and sublittoral zone. The parasite was found in Bovichthys chilensis (Reagan). Auchenionchus variolosus (Valenciennes), Calliclinus genigutattus (Valenciennes), Sindoscopus australis (Fowler and Bean), Myxodes cristatus Valenciennes, and Gobiesox marmoratus (Jenyns). However, only the first species is a suitable host for the parasite as evidenced by the presence of mature females. This acanthocephalan belongs to Arhythmacanthidae, but it does not correspond to any genus described. Spiracanthus bovichthys is different in the number and spiralled distribution of its hooks in the proboscis. In the short proboscis, 3 groups of hooks are distinguished according to size, summing up to 150-190 hooks. The group of largest hooks are found in the apical part of the proboscis, and there are 10 diagonal rows of small hooks from the prebasal to basal proboscis. Its trunk is covered partially by small spines. Amphipod and isopods were the prey items shared among the host fish species and are the best candidates to be the intermediate hosts of S. bovichthys.

Similascarophis n. gen. n. spp. (Nematoda: Cystidicolidae) parasitizing marine fishes off the Chilean coast.

Similascarophis (Cystidicolidae) n. gen. is proposed. In the mouth of specimens of this genus, submedial labia are absent and pseudolabia do not have any part projecting toward the central oral opening. These nematodes were obtained from the alimentary tract of 7 marine fish species along the coast of Chile: Bovichthys chilensis Regan, Eleginops maclovinus (Cuvier), Pinguipes chilensis (Valenciennes), Cilus gilberti (Abbott), Cheilodactylus variegatus Valenciennes, Girella laevifrons (Tschudi), and Graus nigra Philippi. Morphology and morphometry are compared between 2 new Similascarophis species: Similascarophis maulensis n. sp. and S. chilensis n. sp., which differ in the presence of sublabia and in the length of the glandular esophagus and left spicule. We also recorded Similascarophis sp. in 2 other host species, which showed some distinct proportional measurements, although these differences were not sufficiently clear to identify them as a new species.

Species composition of assemblages of Ceratomyxa (Myxozoa), parasites of lings Genypterus (Ophidiidae) in the southeastern Pacific Ocean: an ecomorphometric approach.

Studies on Myxozoa have emphasized their potential impact on aquatic animal health but less on ecological aspects. In this investigation, we assess the importance of host and latitudinal variations in the morphometry of spores of Ceratomyxa Théohan, 1892 (Myxozoa) from the gall bladder of 3 ling Genypterus (Pisces; Ophidiidae) species. Discriminant analyses indicated that several morphospecies of Ceratomyxa coexist in these hosts, despite the fact that the specific level of taxonomic resolution of each spore was not attempted. At least 4 species, i.e., Ceratomyxa hokarari Meglitsch, 1960; Ceratomyxa inversa Meglitsch, 1960; Ceratomyxa laxa Meglitsch, 1960; and Ceratomyxa elongata Meglitsch, 1960 occur in the study area, and at least 2 species co-occur in each host and geographical location. The most widespread pattern found is that spores are larger in golden ling (Genypterus blacodes) and spore size decreases with increasing latitude; this may be associated with the species composition of these assemblages, as well as with the habitat and diet segregation of the host species.

Molecular identification, morphological characterization and new insights into the ecology of larval Pseudoterranova cattani in fishes from the Argentine coast with its differentiation from the Antarctic species, P. decipiens sp. E (Nematoda: Anisakidae).

Larvae of the genus Pseudoterranova constitute a risk for human health when ingested through raw or undercooked fish. They can provoke pseudoterranovosis in humans, a fish-borne zoonotic disease whose pathogenicity varies with the species involved, making their correct specific identification a necessary step in the knowledge of this zoonosis. Larvae of Pseudoterranova decipiens s.l. have been reported in several fish species from off the Argentine coasts; however, there are no studies dealing with their specific identification in this region. Here, a genetic identification and morphological characterization of larval Pseudoterranova spp. from three fish species sampled from Argentine waters and from Notothenia coriiceps from Antarctic waters was carried out. Larvae were sequenced for their genetic/molecular identification, including the mitochondrial cytochrome c oxidase subunit II (mtDNA cox2), the first (ITS-1) and the second (ITS-2) internal transcribed spacers of the nuclear ribosomal DNA, and compared with all species of the P. decipiens (sensu lato) species complex (sequences available in GenBank). Further, adults of Pseudoterranova spp. from the definitive host, the southern sea lion, Otaria flavescens, from Argentine and Chilean coasts were sequenced at the same genes. The sequences obtained at the ITS-1 and ITS-2 genes from all the larvae examined from fish of Argentine waters, as well as the adult worms, matched 100% the sequences for the species P. cattani. The sequences obtained at mtDNA cox2 gene for Antarctic larvae matched 99% those available in GenBank for the sibling P. decipiens sp. E. Both MP and BI phylogenetic trees strongly supported P. cattani and P. decipiens sp. E as two distinct phylogenetic lineages and depicted the species P. decipiens sp. E as sister taxon to the remaining taxa of the P. decipiens complex. Larval morphometry was similar between specimens of P. cattani from Argentina, but significantly different from those of P. decipiens sp. E, indicating that larval forms can be distinguished based on their morphology. Pseudoterranova cattani is common and abundant in a variety of fish species from Chile, whereas few host species harbour these larvae in Argentina where they show low levels of parasitism. This pattern could arise from a combination of factors, including environmental conditions, density and dietary preferences of definitive hosts and life-cycle pathways of the parasite. Finally, this study revealed that the life-cycle of P. cattani involves mainly demersal and benthic organisms, with a marked preference by large-sized benthophagous fish.

The relationship between species richness and productivity in metazoan parasite communities.

Biodiversity is not distributed homogeneously in space, and it often covaries with productivity. The shape of the relationship between diversity and productivity, however, varies from a monotonic linear increase to a hump-shaped curve with maximum diversity values corresponding to intermediate productivity. The system studied and the spatial scale of study may affect this relationship. Parasite communities are useful models to test the productivity-diversity relationship because they consist of species belonging to a restricted set of higher taxa common to all host species. Using total parasite biovolume per host individual as a surrogate for community productivity, we tested the relationship between productivity and species richness among assemblages of metazoan parasites in 131 vertebrate host species. Across all host species, we found a linear relationship between total parasite biovolume and parasite species richness, with no trace of a hump-shaped curve. This result remained after corrections for the potential confounding effect of the number of host individuals examined per host species, host body mass, and phylogenetic relationships among host species. Although weaker, the linear relationship remained when the analyses were performed within the five vertebrate groups (fish, amphibians, reptiles, mammals and birds) instead of across all host species. These findings agree with the classic isolationist-interactive continuum of parasite communities that has become widely accepted in parasite ecology. They also suggest that parasite communities are not saturated with species, and that the addition of new species will result in increased total parasite biovolume per host. If the number of parasite species exploiting a host population is not regulated by processes arising from within the parasite community, external factors such as host characteristics may be the main determinants of parasite diversity.