Taxonomy and ecology of metazoan parasites of otariids from Patagonia, Argentina : adult and infective stages

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At present, the metazoan parasite fauna of most species of otariids is generally poorly known, in part because these marine mammals are mostly protected and, therefore, sampling is limited to specimens stranded on the coast or captured as by-catch in fisheries. Similar problems also occur for the larval stages of gastrointestinal helminths of otariids. For most of these parasite species, the specific identity of the intermediate/paratenic of hosts is unknown and, therefore, many stages of their life cycles remain to be described. Similarly, little is known about the routes of transmission of these parasites between intermediate/paratenic hosts to their otariids definitive hosts. The present thesis is committed to improving the knowledge on these aspects, characterizing for the first time, the intestinal helminth fauna of 56 South American sea lions Otaria flavescens (Shaw, 1800), and 5 South American fur seals Arctocephalus australis (Zimmerman, 1783), from the Patagonian coast of Argentina. Additionally, a total of 542 specimens of 20 marine fish species collected in the same locality, were analysed for helminths, identifying and quantifying the larval forms of parasite infecting otariids. The large dataset obtained provided the opportunity to describe the larval forms and to assess pathways of transmission of these parasites between intermediate/paratenic fish hosts and their definitive otariid hosts. Finally, the large number of larval specimens from several fish species collected in the course of this study allowed us to know essential aspects to understand the population dynamics of these parasites, as the effects of the different host species on some life history traits of the larvae, such as growth patterns or sex ratio, or the potential role of the host in the transmission of the parasite. This study targeted the following objectives: 1) To quantify and describe the intestinal metazoan parasite communities of O. flavescens and A. australis off northern Patagonia, Argentina, based on a detailed morphological and taxonomical study. This information is used to ascertain the role of parasite host specificity in shaping helminth community diversity in otariids. 2) To characterize the component populations of cystacanths of Corynosoma australe (Acanthocephala: Polymorphidae) in paratenic fish hosts off the Patagonian coast of Argentina. The main goal is to elucidate the pathways of transmission of this species between paratenic hosts and definitive otariid hosts, and to assess the effect of different fish hosts on growth, body size, fitness and sex ratio of the cystacanths of C. australe. 3) To describe, for the first time, the temporal allocation of investment on holdfast structures (trunk spines) between cystacanths and adults of two congeneric species of acanthocephalans (Corynosoma cetaceum and C. australe), and investigating the factors that may account for the patterns of trunk spine growth. 4) To carry out a taxonomic identification and description of third-stage larvae of species of Pseudoterranova (Nematoda: Ascaridoidea) from various fish species of Patagonia using sequence data for the mitochondrial cytochrome c oxidase subunit 1 (cox 1) gene and a detailed morphological study. This evidence is then used to describe the component populations of third-stage larvae of species of Pseudoterranova in fishes, assessing the role of different fish hosts on the microhabitat selection, transmission strategies and infection parameters of the third-stage larvae. A total of 97,325 helminth specimens were collected from O. flavescens from the Patagonian coast in Argentina. The intestinal helminth fauna of sea lions in this locality comprised 11 taxa (1 trematode, 1 cestode, 5 nematodes and 4 acanthocephalans). Gravid individuals were represented by 6 species: Ascocotyle (Ascocotyle) patagoniensis, Contracaecum ogmorhini (s.s.), Corynosoma australe, Diphyllobothrium spp., Pseudoterranova cattani and Uncinaria hamiltoni. Third-stage larvae of Anisakis sp. type I and Contracaecum sp., and juvenile specimens of Andracantha sp., Corynosoma cetaceum and Profilicollis chasmagnathi were also collected. Four of these parasites species, Andracantha sp., A. (A.) patagoniensis, C. ogmorhini (s.s.) and P. chasmagnathi represent new host records. A total of 1,516 helminth specimens were collected from the intestine of A. australis. The intestinal helminth fauna of fur seals comprises 7 parasite taxa (2 cestodes, 3 nematodes and 2 acanthocephalans). Gravid individuals were represented by 4 species of parasites: C. ogmorhini (s.s.), C. australe, Diphyllobothrium spp., and P. cattani. Third-stage larvae of Contracaecum sp. and juvenile specimens of C. cetaceum were also collected. Corynosoma australe was the most prevalent and abundant parasite in both hosts, accounting for > 90% of all specimens. In northern Patagonia, sea lions and fur seals harbour the intestinal helminth communities that could be predicted for otariids worldwide, i.e. the combination of species of the genera Corynosoma, Diphyllobothrium, Pseudoterranova, Contracaecum and, in pups, Uncinaria. The estimation of helminth community parameters in sea lions and fur seals, especially species richness at component community level, was affected by the inclusion or exclusion of parasites for which both species of otariids are putative non-hosts (i.e. hosts in which the parasite is unable to reproduce). This study demonstrates that the inclusion of these taxa can exert a significant influence on some community parameters. Information about the reproductive status of helminth species is often lacking in parasitological surveys on otariids and other marine vertebrates, but it is of significance to improve precision in parascript studies or ecological meta-analyses. A new species of a heterophyid trematode was described from the intestine of South American sea lions. A detailed morphological and morphometrical analysis of specimens of Ascocotyle (Ascocotyle) patagoniensis Hernández-Orts, Montero, Crespo, García, Raga and Aznar, 2012 suggests that this trematode can be distinguished from the other species of the subgenus by the number of circumoral spines, which are arranged in 2 rows of 18 to 23, by having a gonotyl without papillae, and by their widest seminal receptacle. Species of the subgenus Ascocotyle usually infect fish-eating birds or mammals in freshwater or brackish habitats. Ascocotyle (A.) patagoniensis is the first species of the subgenus described from a marine mammal. However, no metacercariae of Ascocotyle spp. were found in 542 marine teleosts from 20 species collected along the Patagonian Shelf. The absence of metacercariae in marine fish inhabiting this area could be related to the fact that the life cycle of this trematode is restricted to littoral waters. Nevertheless, more fishes should be analysed to confirm this hypothesis as the small metacercariae could have been overlooked, mainly in host species with small sample sizes. A total of 1,367 cystacanths of C. australe was collected in 18 species of marine fish from the Patagonian coast. The most infected fish species with n ≥ 15 were as follows: Acanthistius patachonicus, Paralichthys isosceles, Prionotus nudigula, Raneya brasiliensis and Xystreurys rasile. Eight fish species, i.e. A. patachonicus, Brama brama, Congiopodus peruvianus, Cottoperca gobio, Genypterus blacodes, Patagonotothen ramsayi, Seriolella porosa and Stromateus brasiliensis represent new host records for C. australe. Results of this study demonstrate that cystacanths of C. australe are able to infect and colonize a wide array of fish species, which would act as paratenic hosts. The ubiquity of this acanthocephalan through the trophic web would guarantee infections to their definitive hosts through alternative pathways. Nevertheless, this study suggest that R. brasiliensis, is one of the prey that most likely contributes to the transmission of cystacanths of C. australe in this area, due to both the high prevalence in this fish species, and its high relative importance in the diet of sea lions and fur seals. There were significant differences in the levels of infection of cystacanths of C. australe between fish inhabiting different zones of the water column, being the ones associated with benthic zone those with highest cystacanth infections. This study suggests that at least 2 main factors could be directly promoting differences in the infection levels of C. australe between fish from different zones: 1) distribution of the invertebrate intermediate hosts; and 2) patterns of transmission of cystacanths between paratenic fish hosts through food webs. The overall sex ratio of cystacanths of C. australe infecting fish hosts was slightly, but significantly, female-biased and no significant differences were found among fish species. This suggests that the sex ratio would begin to be biased before individuals of C. australe infect the definitive host, in which the sex ratio is known to become strongly female-biased because females have a longer life span. In other words, part of the biased sex ratio that we observe in the definitive hosts would be already transferred from paratenic hosts. In theory, 3 factors could be involved in generating the sex ratio biases in our sample, namely, sampling error, differential sampling of female and male larvae, and/or differential mortality between the sexes. This study analyses, for the first time, the potential costs that trophically-transmitted helminths may face in paratenic-to-paratenic transmission. The results suggest that some fish species, in particular Acanthistius patachonicus, might actually be unsuitable paratenic hosts for C. australe since most cystacanths found in this species were not viable. Also, a slight, but statistically significant, tendency to decrease body size of cystacanths was observed as the trophic level of fish species increased. This tendency, which was not related to crowding effects, appears to suggest that C. australe may incur in non-negligible energetic costs when experiencing putative paratenic-to-paratenic transmission. The implications of this finding cannot be underestimated, since this negative consequence may have an important role on the population dynamics of trophically-transmitted helminths. Acanthocephalans have evolved a hooked proboscis and some taxa have trunk spines to attach to their definitive hosts. These structures are generated before being used, thus a key question is how investment in attachment could optimally be allocated through the ontogeny. The number and arrangement of hooks and spines are never modified in the definitive host, but it is unclear whether these structures grow during adult development. The present study compared, for the first time using inferential statistics, the size of holdfast structures between cystacanths and adults of acanthocephalans. The results suggest that the size of trunk spines grows between cystacanths and adults of C. australe and an allied species infecting cetaceans, C. cetaceum, but only in females, which also had significantly larger spines than males. However, this sexual dimorphism did not result from pure allometry since the body of females was smaller, and did not grow more than that of males. Nevertheless, females have longer lifespan, and therefore this factor would induce different investment and development schedules for spines, in order to withstand the extreme flow conditions prevailing in marine mammals for longer time. Unexpectedly, the patterns of spine growth appear also to differ between both species of Corynosoma. In C. cetaceum fore-trunk spines and hind-trunk spines grew, whereas in C. australe only fore-trunk spines differed between cystacanths and adults. An explanation of these differences is that females of C. cetaceum fine-tune the size of spines during the development in the definitive hosts because they achieve a larger adult size, a trait that correlates with stronger dislodging forces and, possibly, with a longer lifespan. This study sheds light on the question of whether or not the holdfast of acanthocephalans is fully developed prior to entering the definitive host. It suggests that temporal allocation of investment in attachment structures may differ, not only between congeneric species, but also between sexes of the same species, possibly due to the different selective pressures that each population subset faces. A total of 635 encapsulated third-stage larvae of Pseudoterranova (sealworm larvae) were collected from 12 species of marine fish from the Patagonian coast. The most infected fish species with sealworm larvae was P. nudigula, followed by A. patachonicus, P. isosceles, Percophis brasiliensis and Pseudopercis semifasciata. Five species of fish, i.e. C. gobio, Nemadactylus bergi, M. argentinae, P. brasiliensis and P. nudigula represent new host records for larval sealworms. Sequences obtained for the mitochondrial cytochrome c oxidase subunit 1 gene (cox 1) of sealworms from the red searobin, P. nudigula, formed a reciprocally monophyletic lineage with published sequences of P. cattani from definitive hosts. A detailed morphological and morphometrical description of larvae of P. cattani from the red searobin is provided. On the other hand, sealworm larvae from other fish species did not differ morphologically from L3 of P. cattani from the red searobin. However, the results of the comparative morphometric analyses carried out on larvae from different fish hosts indicated significant differences in some distances. However, we provisionally identified all larvae as P. cf. cattani, awaiting further identification based on molecular genetic markers. The results of this study suggest that the main microhabitat for sealworm larvae infecting fish hosts from Patagonia is the muscle (principally the epaxial musculature, followed by the hypaxial muscles), and to a lesser degree, in the mesenteries and liver. The lines of evidence obtained in this study suggest that most important fish prey of otariids inhabiting the Patagonian coast presented low infection levels of sealworm larvae. Given that P. cattani is specific to otariids, transmission of this nematode appears to rely on the catholic diet of both sea lions and fur seals, which include a number of specimens of many fish species from the benthic realm, where transmission most likely occurs.
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