The role of parasites in the invasion success of the exotic brine shrimp Artemia Franciscana in the Meditarranean region

Trabajo presentado en el Symposium for European Freshwater Science, celebardo en Girona del 27 de junio al 1 de julio de 2011.Biological invasions are main threats to biodiversity at global scale and increasing numbers of studies suggest that parasites may have a role. However, the mechanism through which parasites may influence the outcome of the invasion is poorly understood. Here we provide evidence supporting the role of parasites as potential agents mediating the competitive exclusion of Mediterranean brine shrimps Artemia (A. parthenogenetica and A. salina) by the exotic American A. franciscana, using different native and invasive populations from South Spain and South France. Our results revealed high rates of infection by cestodes in native brine shrimps, sometimes with extreme prevalences of up to 100%. In contrast, A. franciscana populations showed very low diversity, prevalence and burden of cestodes. The effect of parasites in native populations was multiple, ranging from reproduction and survival, to life history traits, microhabitat selection and diet. Infection strongly reduced host fitness by both, reducing fecundity (parasite castration) and indirectly increasing predation by birds final hosts as revealed by prey choice experiments. We found evidence that high rate of parasitism (particularly the castrating parasite Flamingolepis liguloides, the most prevalent cestode in natives but nearly absent in the exotic Artemia), indirectly affected the life-history strategy of non infected individuals, inducing for example earlier maturation. Moreover cestodes influenced spatial (vertical and horizontal) distribution of the host, altering the diet as revealed by isotopic analysis. Contrasting with the strong impact of parasites in native populations, we have never observed any pathology (castration, behavioural alteration, etc) associated with infection in the exotic species. Overall, the results of this study suggest that the large impact of cestode on the native, but not the invading species, is likely to confer a decisive competitive advantage to the invader, contributing to explain the demographic success of A. franciscana in the Mediterranean region.Peer reviewe

Larval helminths in the invasive American brine shrimp Artemia franciscana throughout its annual cycle

One of the best examples of rapid displacement of native species by an invader is the eradication of native Artemia salina and A. parthenogenetica in the Mediterranean by the introduced American A. franciscana. Previous studies based on sampling from limited time periods suggest that the success of the American species as a competitor may be due partly to different parasite burden, since native Artemia spp. have high cestode infection rates regulating their density. The aim of this study is to test the hypothesis that the helminth infection in A. franciscana in its invasive range is low throughout its annual life cycle. Samples of A. franciscana were collected every second month from La Tapa saltern (Andalusia) during one year. Five helminth species were recorded: cestodes Flamingolepis liguloides, F. flamingo, Gynandrotaenia stammeri (all flamingo parasites), Eurycestus avoceti (a shorebird parasite) and larval spirurids of the Acuariinae (the first record of nematodes in Artemia). The overall infection rate was low, with total prevalence 5.9% and prevalence of individual parasite species between 0.2 and 3.2%. The mean abundance of helminths was 0.005–0.155 (av. 0.068), 5–13 times lower than in native congeners. Waterbird counts indicate that the low infection rates cannot be explained by lack of definitive hosts. The results are consistent with the hypothesis that helminths have no regulating effect on the invasive brine shrimp in the Mediterranean. The replacement of the native populations by the invader can be partially explained by a competition mediated by parasites/predators through a differential impact on host fitnessPeer reviewe

Cestode parasitism in invasive and native brine shrimps (Artemia spp.) as a possible factor promoting the rapid invasion of A. franciscana in the Mediterranean region

Artemia franciscana is an invasive crustacean expanding its range in hypersaline wetlands in the Mediter- ranean region and replacing native Artemia parthenogenetica and Artemia salina. Native brine shrimps are known as intermediate hosts of cestodes; infected individuals exhibit changes in their behaviour and appearance, thus facilitating the parasite transmission to the avian hosts by predation. To assess whether invasive brine shrimps participate in the cestode life cycles to the same extent as the native species, we examined the natural infections in seven populations of Artemia spp. along the southern coast of Spain and Portugal: three populations of each A. franciscana and A. parthenogenetica and one population of A. salina. Ten cestode species were found in A. parthenogenetica, while only six were recorded in each of A. salina and A. franciscana. The overall infection was consistently higher in native than in invasive populations. For a particular cestode species, the prevalence or abundance was significantly higher in a native population for 54 pairwise comparisons and only higher for an invasive population for 4 pairwise comparisons. These results suggest that cestodes may influence competitive interactions between native and invasive brine shrimps, thus partly explaining the invasive success of A. franciscanaPeer reviewe

Red and transparent brine shrimps (Artemia parthenogenetica): a comparative study of their cestode infections

Although the red colour of brine shrimps has previously been supposed to be associated with cestode parasitism, no evidence has been provided that red and transparent brine shrimps differ in their role for cestode circulation. We compared the cestode infections in 100 red and 100 transparent Artemia parthenogenetica collected from the Odiel salt pans in Spain. Seven cestode species were recorded in red, and only four of them were recorded in transparent brine shrimps. The red brine shrimps were more infected with cysticercoids than transparent individuals (prevalence, 87 vs 21%; mean intensity, 1.56 vs 1.00; mean abundance, 1.35 vs 0.21). Three cestode species (Flamingolepis liguloides, Anomotaenia tringae and Confluaria podicipina) had significantly higher prevalence and mean abundance in red brine shrimps. These results suggest that red brine shrimps have a more important role for the circulation of avian cestodes than transparent individuals of the same population.Peer reviewe

Participation of metanauplii and juvenile individuals of Artemia parthenogenetica (Branchiopoda) in the circulation of avian cestodes

Adult crustaceans of the genus Artemia (brine shrimps) are intermediate hosts in the life cycle of cestode species parasitic in aquatic birds as their definitive hosts. However, there are no data on the role of larval and juvenile brine shrimps in the transmission of avian helminth parasites. In order to examine the possible role of early developmental stages (nauplii, metanauplii and juveniles) of Artemia for the circulation of avian cestodes, the natural cestode infection in the population of Artemia parthenogenetica from La Mata Lagoon, Mediterranean coast of Spain, was studied. Metacestodes (cysticercoids) of four cestode species were recorded in adult brine shrimps: Flamingolepis liguloides and Flamingolepis flamingo (hymenolepidids parasitic in flamingos), Confluaria podicipina (a hymenolepidid species parasitic in grebes) and Eurycestus avoceti (a dilepidid species parasitic in avocets, stilts, plovers and, to a lesser extent, in flamingos). No cysticercoids were found in nauplii. Two species, F. liguloides and F. flamingo, were found in metanauplii and juvenile brine shrimps. Only 36.3% of the cysticercoids of F. liguloides occurred in adult brine shrimps; the remaining 63.7% were parasitic in metanauplii (39.6%) and juveniles (24.1%). Similarly, the metacestodes of F. flamingo were also distributed among various age groups: in adults (44.4% of cysticercoids), juveniles (27.8%) and metanauplii (27.8%). These results indicate that the early developmental stages of Artemia have an important role for the circulation of certain parasite species. No cysticercoids of C. podicipina and E. avoceti were recorded in larval and juvenile brine shrimps. The selective infestation of larval brine shrimps with flamingo parasites is probably associated with the feeding behaviour of definitive hosts, which are filtering predators; in contrast, grebes and waders pick brine shrimps individually one by one. The possible underlying mechanism for selective infestation of metanauplii and adults by certain cestode species is associated with the size of parasite eggs, allowing only cestode species with small eggs to be ingested by larval brine shrimps.This work was financed by the Spanish National Plan R & D (project CGL-2005- 02306/BOS) and by the EC-funded project WETLANET to the Institute of Biodiversity and Ecosystem Research, Bulgarian Academy of Sciences. The first author is supported by a Ph.D. grant (FPI) from the Spanish Ministry of Science and Innovation.Peer reviewe

Cestodes from Artemia parthenogenetica (Crustacea, Branchiopoda) in the Odiel Marshes, Spain: A systematic survey of cysticercoids

A total of 3,300 specimens of brine shrimps Artemia parthenogenetica from the Odiel Marshes, Huelva Province, SW Spain, were studied during several seasons of 2002 and 2003 for the presence of cestode infections. Cysticercoids were found in 26.8% of brine shrimps. Eight cestode species were recorded, i.e., Hymenolepididae: Flamingolepis liguloides (adults parasitic in flamingos) with prevalence (P) 18.5%, mean intensity (MI) 1.48 and mean abundance (MA) 0.28; F. flamingo (adults parasitic in flamingos), P 0.9%, MI 1.03, MA 0.01; Confluaria podicipina (adults parasitic in grebes), P 6.5%, MI 1.42, MA 0.09; Wardium stellorae (adults parasitic in gulls), P 0.2%, MI 1.00, MA 0.002; Dilepididae: Eurycestus avoceti (adults parasitic in waders and flamingos), P 2.7%, MI 1.08, MA 0.03; Anomotaenia sp., probably A. microphallos (adults parasitic in waders), P 0.8%, MI 1.04, MA 0.01; A. tringae (adults parasitic in waders), P 2.2%, MI 1.01, MA 0.02; Progynotaeniidae: Gynandrotaenia stammeri (adults parasitic in flamingos), P 0.6%, MI 1.00, MA 0.01. The cysticercoids are described and accompanying illus trations are presented. This study provides the first record of Anomotaenia tringae in an intermediate host and the first records of C. podicipina, E. avoceti, A. tringae and G. stammeri in SpainPeer reviewe

Differential susceptibility to parasites of invasive and native species of Artemia living in sympatry: Consequences for the invasion of A. franciscana in the Mediterranean region

Elucidating the mechanisms making a successful invader remains a central problem in invasion ecology. There is growing evidence supporting that the outcome of competition between species can be controlled by parasites. However our understanding of how parasites affect the interaction between native and invasive species is very limited. Here we explore the role of parasites as potential agents mediating the competitive exclusion of populations of Mediterranean brine shrimps Artemia by the exotic American A. franciscana, which is leading in most of the cases to the extinction of native Artemia populations. We compared the susceptibility of the invasive species and the native A. parthenogenetica to different cestode species using an exceptional case of sympatry in Aigues-Mortes saltern, South of France. The invader A. franciscana showed greatly reduced diversity, low prevalence and low burden of cestode larvae compared to its native congener. Infection in A. parthenogenetica was associated with high fitness costs. In particular, the most prevalent cestode, Flamingolepis liguloides caused castration in A. parthenogenetica. The results of this study suggest that the large impact of cestode on the native, but not the invading species, is likely to confer a decisive competitive advantage to the invader. It thus certainly contributes to explain the demographic success of A. franciscana in the Mediterranean region. © 2012 Springer Science+Business Media B.V.This work has been supported by the ERC grant Quantevol to T. L.Peer Reviewe

Records of cysticercoids of Fimbriarioides tadornae Maksimova, 1976 and Branchiopodataenia gvozdevi (Maksimova, 1988) (Cyclophyllidea, Hymenolepididae) from brine shrimps at the Mediterranean coasts of Spain and France, with a key to cestodes from Artemia spp. From the Western Mediterranean

Cysticercoids of two cestode species isolated from brine shrimps from the Mediterranean coasts of Spain and France are described. Fimbriarioides tadornae Maksimova, 1976 (adults known as parasites of Tadorna tadorna) was recorded from Artemia parthenogenetica and A. franciscana from Spain (Bras del Port and River Ebro Delta, respectively), and from A. franciscana from Aigues-Mortes, France (new geographical record). Branchiopodataenia gvozdevi (Maksimova, 1988) (adults known as parasites of Larus genei) was recorded from A. parthenogenetica (Bras del Port, Spain), A. salina (San Pedro del Pinatar, Spain) and A. franciscana (River Ebro Delta, Spain); this is the first record of the species in Europe. An illustrated key to cysticercoids of 12 cestode species from Artemia spp. from the Western Mediterranean is proposed. © 2009 Versita Warsaw and Springer-Verlag Berlin Heidelberg.This study was partly carried out in the framework of a co-operative project between the Bulgarian Academy of Sciences (BAS) and the Consejo Superior de Investigationes Científicas (CSIC), Spain, entitled "Invasive and native brine shrimps: do cestode parasites control their competitive interactions" (2006-2007). It was also facilitated by visit grants in the frames of the cooperative agreement between CSIC and BAS (2008-2009) and CSIC programme for visiting researchers.Peer Reviewe

High prevalence of cestodes in Artemia spp. throughout the annual cycle: relationship with abundance of avian final hosts

Brine shrimp, Artemia spp., act as intermediate hosts for a range of cestode species that use waterbirds as their final hosts. These parasites can have marked influences on shrimp behavior and fecundity, generating the potential for cascading effects in hypersaline food webs. We present the first comprehensive study of the temporal dynamics of cestode parasites in natural populations of brine shrimp throughout the annual cycle. Over a 12-month period, clonal Artemia parthenogenetica were sampled in the Odiel marshes in Huelva, and the sexual Artemia salina was sampled in the Salinas de Cerrillos in Almería. Throughout the year, 4–45 % of A. parthenogenetica were infected with cestodes (mean species richness = 0.26), compared to 27–72 % of A. salina (mean species richness = 0.64). Ten cestode species were recorded. Male and female A. salina showed similar levels of parasitism. The most prevalent and abundant cestodes were those infecting the most abundant final hosts, especially the Greater Flamingo Phoenicopterus ruber. In particular, the flamingo parasite Flamingolepis liguloides had a prevalence of up to 43 % in A. parthenogenetica and 63.5 % in A. salina in a given month. Although there was strong seasonal variation in prevalence, abundance, and intensity of cestode infections, seasonal changes in bird counts were weak predictors of the dynamics of cestode infections. However, infection levels of Confluaria podicipina in A. parthenogenetica were positively correlated with the number of their black-necked grebe Podiceps nigricollis hosts. Similarly, infection levels of Anomotaenia tringae and Anomotaenia microphallos in A. salina were correlated with the number of shorebird hosts present the month before. Correlated seasonal transmission structured the cestode community, leading to more multiple infections than expected by chance.Peer reviewe