Parasitismo por cestodos en Artemia spp. y su implicación en la invasión biológica de Artemia franciscana en la región Mediterránea

The aim of this Doctoral Thesis is to study parasitism in the crustacean Artemia and cestodes implication in the biological invasion process of the American species Artemia franciscana Kellogg, 1906 in the Mediterranean region. Artemia is the most conspicuous invertebrate in the aquatic hypersaline ecosystems throughout the world, and an important food source for aquatic birds. The use of the American species A. franciscana in aquaculture and pet industries has resulted in their introductions into ecosystems outside of their native range. Consequently, A. franciscana has invaded many hypersaline wetlands all over the world, and it has been recognized as an aquatic global invasive species. In the Western Mediterranean area, this brine shrimp species has become a threat for the native biodiversity (A. salina and A. parthenogenetica), and it has invaded important wetlands as Ramsar sites and Special Protection Areas for birds, provoking a serious conservation problem. Also, Artemia has an essential role for helminth parasites of aquatic birds, mainly cestode cyclophyllidean. This research is a parasitological study in the context of an invasion, with a taxonomical and ecological perspective, and considering aspects related to host-parasite interactions in the Cestodes-Artemia-Birds system. Our work is based in the natural infections by cestodes in Artemia populations from the Mediterranean coast of Spain: A. parthenogenetica (La Mata lagoon, Alicante), A. salina and A. franciscana-introduced (Ebro Delta salterns, Tarragona); and the native A. franciscana population from Great Salt Lake (Utah, USA). We determined the cestode communities and quantified infection levels in the Artemia spp., evaluated the temporal variations of the infections and parasite effects on Artemia colour and reproductive activity. In addition, we explored the influence of several factors as developmental stage, sex and diversity of intermediate host, as well as abundance and distribution of bird final hosts, on the infection patterns. The study on the helminth infections in A. franciscana in Great Salt Lake allowed us to provide the first data of the role of this species as intermediate host for its natural parasites and to compare with the invaded Mediterranean area. Results of this study shown that A. franciscana participates in the life cycle of, at least, five helminth parasites. Four of them are cestodes: three hymenolepidids i.e. Confluaria podicipina (adult parasitic in grebes), Hymenolepis sensu lato californicus (adult parasitic in gulls), Wardium sp. (definitive host unknown, probably charadriiforms birds), and one dilepidid, Furhmannolepis averini (adult parasitic in phalaropes). For the last species, this is the first record in the Nearctic. In addition, an unidentified nematode of the family Acuariidae was recorded. The overall cestode infection in this native population of A. franciscana in Great Salt Lake is much higher than in the introduced populations of the same host in the Palaearctic region. This result is in agreement with the hypothesis that A. franciscana has a lower susceptibility to the Palaearctic cestode parasites than to cestode parasites in its native range. It suggests that the American brine shrimp is lower regulated by parasites, explaining (at least partially) its higher demographic growth in invaded habitats where it become an invasive species. The species composition of helminth parasites and the spatial variations in their prevalence and abundance may reflect the abundance and distribution of aquatic birds serving as definitive hosts. Concerning the influence of certain factors in the infections, our results indicate that age (in terms of developmental stage) of the intermediate host determines patterns of infection. We found cestode cysticercoids in all developmental stages of brine shrimps except in nauplii. In general, overall infection rates are higher in adults than in metanauplii and juvenile individuals, suggesting an accumulative effect of parasites with advancing host development. In fact, we demonstrated that earlier developmental stages of Artemia have an important role for the circulation of certain parasites species, particularly flamingo parasites (Flamingolepis liguloides and Flamingolepis flamingo). This is probably associated with the feeding behaviour of definitive hosts (filtering versus picking predators), and, also, with the size of parasite eggs and the filtering ability of brine shrimps. Our results demonstrate that A. franciscana has accumulated novel parasites following its introduction. In fact, the invasive species A. franciscana inhabiting the Ebro Delta salterns is characterized by a more diverse assemblage than those observed in other areas of the introduced or native range. We recorded ten cestode species: Flamingolepis liguloides, Flamingolepis flamingo, Wardium stellorae, Branchiopodataenia gvozdevi, Fimbriarioides tadornae (Hymenolepididae); Eurycestus avoceti, Anomotaenia tringae, Anomotaenia microphallos (Dilepididae); Gynandrotaenia stammeri, Gynandrotaenia sp. (Progynotaeniidae). This is also the first record for W. stellorae (a cestode specific of gulls) in this alien brine shrimp. We found a differential infection rate and distribution of cestode species between age groups, suggesting age effect and a relation with final host feeding behaviour. For this exotic host, E. avoceti (parasite of shorebirds) and F. flamingo (flamingo parasite) were the most prevalent and abundant cestodes in adult and juveniles, respectively. Comparing with native range (USA), overall rate of cestode infection in this exotic brine shrimp was much lower. The lower burden of parasites in introduced host suggests A. franciscana is resistant to several native cestode species (such as F. liguloides). Also, when comparing cestode infections between native A. salina and invader A. franciscana from syntopic populations, we found that native host had consistently higher infection parameters, largely because the dominant cestode in A. salina (F. liguloides) was much rarer in A. franciscana. The abundance of E. avoceti and F. liguloides was higher in the A. franciscana population coexisting with A. salina species than when alone, possible because native shrimp provides a better reservoir for parasite circulation. Infection by cestodes caused red colouration and castration in A. salina and A. franciscana, however both these effects were significantly stronger in the native host. The reduced levels of infection and reduced castration effects in A. franciscana suggest that cestodes may not be able to infect or manipulate the alien host to a sufficient extent to ensure viability of parasite populations. The reduced redness suggests that cestode are less likely to reach final hosts (through bird predation) when infecting alien Artemia. The lower regulation and manipulation by parasites likely help A. franciscana outcompete native Artemia species. Resistance to cestodes could be explaining its invasiveness in the Ebro Delta salterns and other invaded ecosystems across the Old World. The results of this Doctoral Thesis highlight the essential role of Artemia as intermediate host for helminth parasites of aquatic birds, A. salina and A. parthenogenetica in the Palaearctic as well A. franciscana in the Nearctic, and contribute to better knowledge of parasitism in Artemia spp., providing first data in America. In other hand, we provide significant information under a conservationist point of view. Considering the importance of Artemia in the trophic web of hypersaline wetlands, the provided knowledge on the invasiveness of this American crustacean in natural conditions and the implications of cestodes in the successful invasion, shed light on the ecological consequences of this biological invasion. In summary, this Thesis allowed us to provide knowledge of host-parasite interactions in the context of the aquatic invasions, in particular, to understand the invasion process of A. franciscana in the Mediterranean region. The invasion of this alien brine shrimp has provoked a biodiversity loss of the genus Artemia, but its impacts may extend to native biota of aquatic hypersaline ecosystems, affecting different levels of biotic interactions: host-parasite and prey-predator. Dramatic consequences of this biological invasion reveal the need to establish urgent measures of control and management to avoid the A. franciscana expansion. In other hand, this Thesis proposes a new study model to be considered in parasitological field.