Dr. George-Nascimento-Failla, Mario

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.

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, Viñ a 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 Viñ a 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.

Parasites alter the reproductive performance of their hosts, limit their growth, and thereby modify the energy budget of these hosts. Experimental studies and theoretical models suggest that the outcome of the host-parasite interactions could be determined by ecological factors such as food availability levels in the local habitats. Nutrient inputs may affect the host's food resource availability with positive or negative effects on parasite infection rates and tolerance of infection, however this has not been specifically evaluated in natural systems. In this study, we evaluate the effects of parasitism by Proctoeces humboldti on body size, gonadosomatic index (GSI), and metabolic rate (oxygen consumption) of their second intermediate host Fissurella crassa limpets, under contrasting natural conditions of productivity (upwelling center vs upwelling shadow sites). Our results evidenced that parasitized limpets collected from the intertidal habitat influenced by coastal upwelling site showed greater shell length, muscular foot biomass and GSI as compared to non-parasitized limpets collected in the same site, and compared to parasitized and non-parasitized limpets collected from the sites under the influence of upwelling shadow conditions. Oxygen consumption was lower in parasitized limpets collected from the upwelling-influenced site than in the other groups, independent of age, suggesting reduced metabolic stress in infected individuals inhabiting these productive sites. Our results suggest that increased productivity in upwelling sites could mitigate the conflict for resources in the P. humboldti – F. crassa system, influencing where such interaction is found in the continuum between parasitism and mutualism. Since parasitism is ubiquitous in natural systems, and play important roles in ecological and evolutionary processes, it is important to analyze host-parasite interaction across a variety of ecological conditions, especially in biological conservation.

Hookworms of the genus Uncinaria parasitize pinniped pups in various locations worldwide. Four species have been described, two of which parasitize pinniped pups in the southern hemisphere: Uncinaria hamiltoni parasitizes Otaria flavescens and Arctocephalus australis from the South American coast, and Uncinaria sanguinis parasitizes Neophoca cinerea from the Australian coast. However, their geographical ranges and host specificity are unknown. Uncinaria spp. are morphologically similar, but molecular analyses have allowed the recognition of new species in the genus Uncinaria. We used nuclear genetic markers (internal transcribed spacer (ITS) and large subunit (LSU) rDNA) and a mitochondrial genetic marker (cytochrome c oxidase subunit I (COI)) to evaluate the phylogenetic relationships of Uncinaria spp. parasitizing A. australis and O. flavescens from South American coasts (Atlantic and Pacific coasts). We compared our sequences with published Uncinaria sequences. A Generalized Mixed Yule Coalescent (GMYC) analysis was also used to delimit species, and principal component analysis was used to compare morphometry among Uncinaria specimens. Parasites were sampled from A. australis from Peru (12°S), southern Chile (42°S), and the Uruguayan coast, and from O. flavescens from northern Chile (24°S) and the Uruguayan coast. Morphometric differences were observed between Uncinaria specimens from both South American coasts and between Uncinaria specimens from A. australis in Peru and southern Chile. Phylogenetic and GMYC analyses suggest that south-eastern Pacific otariid species harbour U. hamiltoni and an undescribed putative species of Uncinaria. However, more samples from A. australis and O. flavescens are necessary to understand the phylogenetic patterns of Uncinaria spp. across the South Pacific.

Galaxias maculatus is an abundant freshwater fish species in Chilean continental waters where it plays important ecological functions, yet few parasitological records of this species exist in Chile and all of them cover a very limited geographic range. The objective of this study was to assess large scale geographic variation in composition of parasite infracommunities of Galaxias maculatus. Specifically, parasite infracommunities of this species were compared among 11 locations across 9 degrees of latitude and 3 ecosystem types (lake, river and estuary). Most taxa found had been previously reported in Chile and Argentina. However, this is the first report for Tylodelphys sp. in this host in Chile. Furthermore, the cranial parasite Tylodelphys sp. had the highest overall prevalence and abundance compared to other parasite species. Despite the fact that the abundance of Tylodelphys sp. was not significantly correlated with Fulton’s condition factor of fish, infected fish seem to have a better body condition compared to uninfected ones. The most important source of variation in composition of infracommunities was the sampling location. Furthermore, fish from lakes have a different composition of parasite infracommunities mainly due to higher abundances of Tylodelphys sp.

Biological interactions and environmental constraints alter life-history traits, modifying organismal performances. Trematode parasites often impact their hosts by inducing parasitic castration, frequently correlated with increased body size in the host (i.e., gigantism hypothesis), which is postulated to reflect the re-allocation of energy released by the reduction in the reproductive process. In this study, we compared the effect of a trematode species on shell size and morphology in adult individuals of the intertidal mussels Perumytilus purpuratus (>20 mm) collected from two local populations of contrasting environmental regimes experienced in central-southern Chile. Our field data indicates that in both study locations, parasitized mussels evidenced higher body sizes (shell length, total weight and volume) as compared with non-parasitized. In addition, parasitized mussels from the southern location evidenced thinner shells than non-parasitized ones and those collected from central Chile, suggesting geographical variation in shell carbonate precipitation across intertidal habitats of the Chilean coast. In laboratory conditions, mussels collected from a local population in central Chile were exposed to two temperature treatments (12 and 18 °C). Parasitized mussels showed higher growth rates than non-parasitized, regardless of the seawater temperature treatments. However, the metabolic rate was not influenced by the parasite condition or the temperature treatments. Our field and laboratory results support the parasite-induced gigantism hypothesis, and suggest that both the thermal environment and geographic location explain only a portion of the increased body size, while the parasitic condition is the most plausible factor modulating the outcome of this host-parasite interaction.

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.

Notothen fishes (Nototheniidae) have been recorded on the coasts of South America, from 35°S to southern. Little is known about the biology of intertidal notothen fishes or their relationships with other species, including parasites. Here, we analyzed the parasitic fauna of a species of Notothenia collected from the rocky intertidal of Lebu, south-central Chile (36°S) and compared the parasite community of this host with other 9 fish species commonly found in rocky intertidal pools. Among the tested species, Notothenia sp. had the highest parasite richness (21 parasitic taxa vs. 1 to 9 parasitic taxa). The composition of parasite species was different among fishes, with similarity indices between 0 and 33%. The parasite composition of Notothenia sp. was most similar to Calliclinus geniguttatus (27%). The most abundant and prevalent parasites found in Notothenia sp. were the copepod Caligus cf. cheilodactyli, Tetraphyllidea larvae, anisakid nematodes, and several acanthocephalan species, which are typical of other fish from the subtidal and bento-demersal zones. Therefore, we conclude that the juveniles of Notothenia sp. were a few months old and had their parasites when reaching the intertidal zone, acquired some generalist parasites during their stay in this habitat, such as Holobomolochus chilensis and Lecithaster macrocotyle. Most notothen fishes are from Antarctic and Sub-Antarctic waters, therefore, it is possible that this fish came from another habitat but also from the austral region of South America. Notothenia sp. could not be specifically identified because of different results between morphological and genetic analyses.

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 coasts of central Chile and central California are important points of comparison in the study of ecological convergence such as a host’s parasite load because of their similar environmental conditions and the shared presence of many families of different species. In this study, the diversity of parasites in fish species from both zones was analyzed and compared to establish if there are similarities between them. The presence of 6 taxonomic groups of parasites was determined using published literature and databases for each location. A presence-absence matrix was created for the fish species studied in Chile and California, and a similarity analysis was carried out to prove whether the parasite loads of both zones were similar. The parasite taxa most frequently found in fish in central California were Digenea and Nematoda, whereas in central Chile the common taxa were Digenea, Annelida, Copepoda, Acanthocephala, and Nematoda. The similarity analysis showed that the parasite composition was different between zones. Nevertheless, overlaps were obtained in the parasitic diversity grouping the host in 3 host groups, one of which consists of hosts from both zones. This difference can be explained by the low parasitic diversity in the assemble of rocky intertidal fishes in California, potentially due to the limited amount of existing studies on intertidal fish parasites in California, along with other possible factors not explored in the present study.