Marta I. Sánchez

Implications of waterbird ecology for the dispersal of aquatic organisms

In this paper, we review some potential implications of waterbird ecology for their role as dispersers of aquatic plants and invertebrates. We focus particularly on internal transport (endozoochory) by the Anatidae (mainly ducks) and shorebirds, groups especially important for dispersal processes owing to their abundance, migratory habitats and diets. We conduct a literature review to assess the seasonal patterns shown by Anatidae in consumption of seeds and plankton, the interspecific patterns in such consumption (including the effects of body size, bill morphology, etc.), and differences in habitat use (e.g., shoreline vs. open water specialists) and migration patterns between species (e.g., true migrants vs. nomads). We show that many shorebirds are important consumers of seeds as well as plankton, and suggest that their role in plant dispersal has been underestimated. This review confirms that Anatidae, shorebirds and other waterbirds have great potential as dispersers of aquatic organisms, but illustrates how closely related, sympatric bird species can have very different roles in dispersal of specific aquatic organisms. Furthermore, great spatial and temporal variation is likely in dispersal patterns realized by a given bird population. We present evidence suggesting that northbound dispersal of aquatic propagules by endozoochory during spring migration is a frequent process in the northern hemisphere. Much more systematic fieldwork and reanalysis of the existing data sets (e.g., from diet studies) are needed before the relative roles of various waterbird species as dispersers can be fully assessed.

The American brine shrimp as an exotic invasive species in the western Mediterranean

The hypersaline environments and salterns present in the western Mediterranean region (including Italy, southern France, the Iberian Peninsula and Morocco) contain autochthonous forms of the brine shrimp Artemia, with parthenogenetic diploid and tetraploid strains coexisting with the bisexual species A. salina. Introduced populations of the American brine shrimp A. franciscana have also been recorded in these Mediterranean environments since the 1980s. Based on brine shrimp cyst samples collected in these countries from 1980 until 2002, we were able to establish the present distribution of autochthonous brine shrimps and of A. franciscana, which is shown to be an expanding invasive species. The results obtained show that A. franciscana is now the dominant Artemia species in Portuguese salterns, along the French Mediterranean coast and in Cadiz bay (Spain). Co-occurrence of autochthonous (parthenogenetic) and American brine shrimp populations was observed in Morocco (Mar Chica) and France (Aigues Mortes), whereas A. franciscana was not found in Italian cyst samples. The results suggest these exotic A. franciscana populations originate as intentional or non-intentional inoculations through aquacultural (hatchery effluents) or pet market activities, and suggest that the native species can be rapidly replaced by the exotic species.

Global ecological impacts of invasive species in aquatic ecosystems

The introduction of invasive species, which often differ functionally from the components of the recipient community, generates ecological impacts that propagate along the food web. This review aims to determine how consistent the impacts of aquatic invasions are across taxa and habitats. To that end, we present a global meta-analysis from 151 publications (733 cases), covering a wide range of invaders (primary producers, filter collectors, omnivores and predators), resident aquatic community components (macrophytes, phytoplankton, zooplankton, benthic invertebrates and fish) and habitats (rivers, lakes and estuaries). Our synthesis suggests a strong negative influence of invasive species on the abundance of aquatic communities, particularly macrophytes, zooplankton and fish. In contrast, there was no general evidence for a decrease in species diversity in invaded habitats, suggesting a time lag between rapid abundance changes and local extinctions. Invaded habitats showed increased water turbidity, nitrogen and organic matter concentration, which are related to the capacity of invaders to transform habitats and increase eutrophication. The expansion of invasive macrophytes caused the largest decrease in fish abundance, the filtering activity of filter collectors depleted planktonic communities, omnivores (including both facultative and obligate herbivores) were responsible for the greatest decline in macrophyte abundance, and benthic invertebrates were most negatively affected by the introduction of new predators. These impacts were relatively consistent across habitats and experimental approaches. Based on our results, we propose a framework of positive and negative links between invasive species at four trophic positions and the five different components of recipient communities. This framework incorporates both direct biotic interactions (predation, competition, grazing) and indirect changes to the water physicochemical conditions mediated by invaders (habitat alteration). Considering the strong trophic links that characterize aquatic ecosystems, this framework is relevant to anticipate the far-reaching consequences of biological invasions on the structure and functionality of aquatic ecosystems.

Passive internal dispersal of insect larvae by migratory birds

It has long been assumed that the resistant eggs of many zooplankton are able to survive passage through the gut of migratory waterbirds, thus facilitating their dispersal between isolated aquatic habitats. We present the first evidence that such passive internal transport within birds may be relevant for insect populations. In three out of six faecal samples from black-tailed Godwits on autumn migration in southwest Spain, we found larvae of the chironomid Chironomus salinarius which had survived gut passage. Although adult chironomids can fly, they are likely to disperse greater distances when transported as larvae via birds. In insects with discrete generations, such passive transport also enables colonization of new habitats at times when flight by adults is not an option.

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 Mediterranean 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. franciscana.

Temporal and spatial variation of an aquatic invertebrate community subjected to avian predation at the Odiel salt pans (SW Spain)

We studied the temporal variation in abundance and distribution of inverte- brates in the water column in both traditional and industrial salt pans in the Odiel marshes, south-west Spain, in 2001. We selected 12 ponds that were representative of different salinities and stages of salt production. Every two months, invertebrates were sampled within the 0 - 20 cm depth range used by foraging waders. We identified 40 taxa, including 30 aquatic and eight terrestrial metazoan invertebrates. Aquatic inverte- brate taxa richness and diversity decreased significantly with increasing pond salinity, whereas total biomass showed a non-significant increase. Overall, Artemia partheno- genetica constituted 67.6 % of invertebrates by number, and 95.5 % of the biomass. The copepod Cletocamptus retrogressus represented 31.1 % of invertebrates by num- ber, and 0.6 % of the biomass. Invertebrate biomass and dominance of A. parthenogen- etica was highest in September and lowest in November. There was significant spatial and temporal variation in abundance for all aquatic taxa, and for a given pond and month, the depth, distance to shoreline and fetch (wind effects) all had important par- tial effects on invertebrate distribution. Ordination methods showed a strong relation- ship between community structure and water chemistry (salinity, pH and redox poten- tial), with the salinity gradient being the most important. There was a clear separation between low salinity ponds with fish and submerged macrophytes and other ponds. The more intensively managed industrial salines held lower densities and biomass of invertebrates than traditional salines, perhaps owing to greater protection from wind or greater inputs of detritus. The beetle Ochthebius corrugatus was abundant in the tradi-

Seasonal variation in the diet of Redshank Tringa totanus in the Odiel Marshes, southwest Spain: a comparison of faecal and pellet analysis

Capsule Redshank diet from southern Europe during migration shows spatial and seasonal variations. Aims To assess seasonal variation in Redshank diet at a major passage site, and to compare data derived from analysing pellets or faeces. Methods At the Odiel Marshes in 2001, pellets from spring migration (39), autumn migration (121) and midwinter (15) were analysed, together with faecal samples from autumn (84). Results The abundance of different invertebrate groups in pellets varied between seasons. In spring, Chironomus salinarius pupae and larvae dominated by volume, followed by Ephydridae larvae and the beetle Paracymus aenus. Polychaetes and molluscs dominated in autumn, and isopods in midwinter. In autumn, chironomid larvae, Mesembryanthemum nodiflorum seeds and Artemia cysts were relatively more abundant in faeces, whereas polychaetes, isopods, molluscs and cestode cysticercoids were more abundant in pellets. Harder and/or larger items were thus relatively more abundant in pellets than faeces. Pellet analysis gave more emphasis to mudflat prey, and faeces to saltpan prey. Conclusion Pellet and faecal analysis give different results for wader diet, and it is useful to combine the two methods. However, they show significant correlations both in diet range and rank abundance of prey items. Redshank diet shows much seasonal and spatial variation in southern Europe.

NEUROLOGICAL AND PHYSIOLOGICAL DISORDERS IN ARTEMIA HARBORING MANIPULATIVE CESTODES

Abstract There are many impressive examples of host manipulation by parasites, but mechanisms underlying these ethological changes, as well as their physiological consequences, are not well characterized. Here, we analyzed part of the cerebral proteome of brine shrimp Artemia infected by manipulative cestodes, using for the first time the ProteinChip Surface-Enhanced Laser Desorption Ionization and Time of Fly Mass Spectrometry (SELDI-TOF MS) system, which has been proposed as an excellent way to analyze the host genome during the host–parasite interaction processes. We found 2 peptides downregulated in individuals infected by the dilepidid, Anomotaenia tringae (4.5 kDa), and by the 2 hymenolepidids, Flamingolepis liguloides and Confluaria podicipina (3.9 kDa), which are potential candidates for involvement with the manipulation process. The identification of 2 head peptides (4.1 and 4.2 kDa) overexpressed in all the categories in brine shrimp living at the surface (both infected individuals and uninfected controls) suggests its association with the different environmental conditions experienced at the water surface. In parallel, brine shrimp infected by C. podicipina showed significant values of triglycerides, potentially augmenting their profitability and attractiveness for the predaceous definitive host (grebes). We discuss our findings in relationship with current ideas on the complexity of parasitically modified organisms.

The diets of the White-headed Duck Oxyura leucocephala, Ruddy Duck O. jamaicensis and their hybrids from Spain

We studied the gut contents of 17 White-headed Ducks, 25 North American Ruddy Ducks and 26 hybrids between the two species collected from 14 Spanish wetlands. This is the most detailed study to date of Oxyura diet in the Palearctic region. Food items from at least 27 families of invertebrates and at least ten families of aquatic plants were identified. The method of collection of ducks and rapid digestion of soft-bodied invertebrates may have overestimated the importance of plant matter. However, animal foods were more important, constituting 73% of aggregate volume of gullet contents. In both duck species and their hybrids, benthic chironomid larvae and pupae were the most important food item, present in 69% of gullets and 75% of gizzards, and constituting 35% of aggregate volume and 26% of aggregate percentage in gullets. Angiosperm seeds were the next most important dietary component, and crustaceans (mainly Amphipoda, Cladocera and Isopoda) and green plant material were of secondary importance. No significant differences in diet were detected between duck species, sex or age classes. Birds sampled in the breeding season had more nematodes, but these may have been parasitic. Chironomids were less abundant in Ruddy Ducks collected from northern Spain outside of the range of the White-headed Duck.

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.