Luísa Mendes

Variation in the innate and acquired arms of the immune system among five shorebird species.

SUMMARY To contribute to an understanding of the evolutionary processes that shape variation in immune responses, we compared several components of the innate and acquired arms of the immune system in five related, but ecologically diverse, migratory shorebirds (ruff Philomachus pugnax L., ruddy turnstone Arenaria interpres L., bar-tailed godwit Limosa lapponica L., sanderling Calidris alba Pallas and red knot C. canutus L.). We used a hemolysis-hemagglutination assay in free-living shorebirds to assess two of the innate components (natural antibodies and complement-mediated lysis), and a modified quantitative enzyme-linked immunosorbent assay in birds held in captivity to assess the acquired component (humoral antibodies against tetanus and diphtheria toxoid) of immunity. Ruddy turnstones showed the highest levels of both innate and acquired immune responses. We suggest that turnstones could have evolved strong immune responses because they scavenge among rotting organic material on the seashore, where they might be exposed to a particularly broad range of pathogens. Although ruffs stand out among shorebirds in having a high prevalence of avian malaria, they do not exhibit higher immune response levels. Our results indicate that relationships between immune response and infection are not likely to follow a broad general pattern, but instead depend on type of parasite exposure, among other factors.

Avian malaria infections in western European mosquitoes

In the complex life cycle of avian malaria parasites (Plasmodium sp.), we still have a poor understanding on the vector–parasite relationships. This study described the community of potential avian malaria vectors in four Portuguese reedbeds. We tested if their geographical distribution differed, and investigated on their Plasmodium infections. The mosquitoes’ feeding preferences were evaluated using CO2, mice, and birds as baits. The most abundant species were Culex pipiens, Culex theileri, and Ochlerotatus caspius (and, in one site, Coquillettidia richiardii). Plasmodium lineages SGS1 and SYAT05 were found in unengorged Cx. pipiens and Cx. theileri, respectively, suggesting that these mosquitoes were competent vectors of those lineages. The species’ abundance was significantly different among sites, which may help to explain the observed differences in the prevalence of SGS1. At the study sites, SGS1 was detected in the most abundant mosquito species and reached a high prevalence in the most abundant passerine species. Probably, this parasite needs abundant hosts in all phases of its cycle to keep a good reservoir of infection in all its stages. Cq. richiardii showed an opportunistic feeding behavior, while Cx. pipiens appeared to be more mammophilic than previously described, perhaps because the used avian bait was not its preferential target. In one of the study sites, mosquitoes seem to be attracted to the Spotless Starling Sturnus unicolor, an abundant bird species that may be an important local reservoir of avian malaria infections. To our knowledge, this is the first report of detection of avian Plasmodium DNA from European mosquitoes.

Host-parasite associations and host-specificity in haemoparasites of reed bed passerines.

The host specificity and host sharing of avian haemoparasites (genera Haemoproteus and Plasmodium) is still poorly known, although they infect a large proportion of several studied bird populations. This study used molecular techniques to detect haemoparasites in marsh warblers and in other passerines that feed in reed beds, at 4 sites in Portugal. The host-specificity of the parasite lineages was analysed and compared with other cases described in the literature to assess whether apparent host specificity changes according to the studied system. Nine lineages of Haemoproteus and 15 of Plasmodium were found, of which only 10 Plasmodium were proven to have local transmission. Each lineage was confined to a distinct set of host species. The distribution of parasites in the host species was non-nested, meaning that specialist lineages did not always share hosts with generalists. The most prevalent lineages were those with a wider host range, indicating that the ability to infect more hosts will enhance a parasites prevalence in its entire host range. We also found that in our areas, a specialist parasite (H. MW1) appears to have a more generalist character than described in the literature, suggesting that a parasites apparent specialization can depend on the type of host species sampled.

Hidden haemosporidian infections in Ruffs (Philomachus pugnax) staging in Northwest Europe en route from Africa to Arctic Europe

In their African freshwater wintering habitats, shorebirds show a high prevalence of blood parasites, whereas no parasites are detected elsewhere along the migration route. We looked at two genera of haemosporidian parasites, Haemoproteus and Plasmodium, in the long-distance migrating Ruff (Philomachus pugnax) along a geographical/seasonal gradient to verify the infection pattern and examine possible hidden organ infections at European staging areas. We amplified parasite DNA from blood of 53 healthy birds wintering in Mali, 53 samples of seven organ tissues (spleen, liver, kidneys, heart, lungs, brain, and pectoral muscle) from healthy individuals caught during spring migration, and 18 weak birds found sick in summer in The Netherlands. We confirm that Ruffs wintering in Africa carried blood infections and that some infections developed into hidden organ infections during spring migration. Moreover, sick birds either had new infections (in one juvenile) or relapses (in an adult harboring an African lineage). Our results suggest that some parasites develop latency. This strategy may be beneficial for the parasite as it may take control over reappearance in the blood to help further transmission.

Local haemoparasites in introduced wetland passerines

AbstractWhen colonizing a new area, introduced species may lose their original haemoparasites. If the local parasites are unable to infect the novel introduced hosts, these may gain a fitness advantage over their local competitors. Alternatively, the introduced species may be susceptible to local parasites and enter the local transmission dynamics. We studied these two possibilities in communities of wetland passerines infected with haemosporidians (genera Haemoproteus and Plasmodium) in Portugal, southwest Europe. Four introduced and six native (resident and breeding migrant) passerine species were tested for haemosporidians in four reed beds. Our results suggest that the introduced species have lost their original haemoparasites upon colonization and entered the local transmission cycle. Two local Plasmodium lineages infected the exotic species: one of them (SGS1) was the most host generalist and prevalent lineage in the native species, so was expected to be present in the exotics at random. The other lineage (PADOM01) was rarer in the sampled community, but was present in native hosts that are phylogenetically close to the infected exotic species; therefore, the colonization of the exotic host by PADOM01 seems to be constrained by the parasite’s specialization and by phylogenetic factors. When phylogeny was controlled for, there were no significant differences in infection prevalence and number of lineages between exotics and natives.ZusammenfassungLokale Blutparasiten bei neu zugezogenen Sperlingsvögeln in Feuchtgebieten Neu eingebürgerte Arten verlieren möglicherweise ihre originalen Blutparasiten, wenn sie ein neues Gebiet besiedeln. Sind die örtlichen Parasiten nicht in der Lage, die neu zugezogenen Wirte zu infizieren, gewinnen diese womöglich einen Fitness-Vorteil gegenüber ihren ortsansässigen Konkurrenten. Andererseits sind die neuen Arten vielleicht aber auch empfänglich für die örtlichen Parasiten und geraten dann in die örtliche Übertragungs-Dynamik. Wir untersuchten diese beiden Alternativen bei Gruppen von Feuchtgebiets-Sperlingsvögeln in Portugal, Südwest-Europa, die mit Haemosporidien (Haemoproteus und Plasmodium) infiziert waren. In vier Schilfgürteln wurden vier neu angesiedelte sowie sechs lokale (ortsansässige und brütende Zugvögel) Sperlingsvogelarten auf Haemosporidien getestet. Unsere Ergebnisse legen nahe, dass die neu zugezogenen Arten nach der Besiedelung ihre ursprünglichen Blutparasiten verloren und in die örtlichen Übertragungs-Zyklen gerieten. Zwei lokale Plasmodium-Verwandtschaftslinien infizierten die neu angesiedelten Arten: eine davon (SGS1) war der größere Wirts-Generalist und in den ortsansässigen Arten am weitesten verbreitet; wir erwarteten, dass er in den neu angesiedelten Arten zufällig verteilt war. Die andere Linie, PADOM01, trat in der Testgruppe seltener auf, war aber in denjenigen ortsansässigen Wirten vorhanden, die den angesiedelten, infizierten Arten phylogenetisch nahe standen. Demnach scheint die Kolonisierung der angesiedelten Wirtsvögel durch PADOM01 durch die Spezialisierung des Parasiten sowie durch phylogenetische Faktoren eingeschränkt zu sein. Ein Test der Phylogenie zeigte zwischen angesiedelten und ortsansässigen Tieren keine signifikanten Unterschiede in der Verbreitung der Infektionen und der Anzahl der Verwandtschaftslinien.

Borrelia garinii and Francisella tularensis subsp. holarctica detected in migratory shorebirds in Portugal

Migratory shorebirds use, among many, the East Atlantic Flyway that links breeding areas as north as Tundra habitats to aquatic wintering grounds in West Africa. As a consequence, they are potentially important in the spread of global zoonotic diseases transmitted by ticks, such as Lyme borreliosis and tularemia—two diseases previously detected in Portugal. In this study, we looked at the infection status of seven populations of shorebirds during their migration, breeding, or wintering in the Portuguese wetlands to access if they carry these pathogens and to discuss their potential risk in the Portuguese wetlands. A total of 212 migratory shorebirds captured in the Tagus and Sado estuaries; key staging and wintering sites in this flyway and important breeding areas for some species were analyzed for the presence of Borrelia burgdorferi sensu lato and Francisella tularensis. In the present study, B. garinii was identified in seven (3%) specimens (five black-tailed godwits Limosa limosa, one common redshank Tringa totanus, and one little stint Calidris minuta), whereas F. tularensis subsp. holarctica was identified in one (0.4%) little stint. To our knowledge, this is the first evidence that shorebirds that migrate through or winter in Portugal transport these pathogens, potentially contributing for their introduction along the flyway, including the Mediterranean region.

Characterization of haemosporidian infections in warblers and sparrows at south-western European reed beds

AbstractThe prevalence and intensity of avian haemosporian infections (genera Haemoproteus and Plasmodium) were investigated using molecular techniques and microscopy in nine passerine species at three Portuguese reed beds along a small latitudinal gradient. The effect of age, sex, season, site and year in the infection prevalence was evaluated for some of these host species. Of the sampled birds, 34.5% were infected, all with low level parasitemias. Haemoproteus spp. was only present in migrant species and was not locally transmitted, while Plasmodium spp. infected more species and reached a higher overall prevalence. Prevalence differed among bird species and was affected by different variables for each species: it was associated with age in the Reed Warbler Acrocephalus scirpaceus, with season in the Cetti’s Warbler Cettia cetti and with year in the House Sparrow Passer domesticus. Site did not influence prevalence for any species at this small geographical scale. Reed Warbler adults had already migrated to Africa and contacted with two different parasite faunas, whereas juveniles had not, thereby explaining the importance of age to explain parasitemia in this species. For the resident Cetti’s Warbler, prevalence varied significantly with season, perhaps due to lower food availability in autumn and winter, making birds weaker and more prone to infection.ZusammenfassungCharakterisierung von Haemosporida Infektionen in Grasmücken und Sperlingen in Röhrichtgebieten in SW-Europa Wir untersuchten die Prävalenz und die Intensität des Vorkommens von Haemosporidien (Gattungen Haemoproteus und Plasmodium) in neun Singvogelarten in drei Portugiesischen Röhrichtgebieten entlang eines geringen Nord-Süd Gradienten. Wir evaluierten die Effekte von Alter, Geschlecht, Jahreszeit, Gebiet und Jahr auf die Prävalenz der Infektionen für einige der Arten. 34,5% der beprobten Vögel waren infiziert, alle mit geringer Parasitämie. Haemoproteus ssp. war nur in Zugvogelarten präsent und wurde nicht lokal übertragen, während Plasmodium ssp. mehrere Arten infizierte und insgesamt eine höhere Prävalenz erreichte. Die Prävalenz zwischen verschiedenen Arten war unterschiedlich hoch, und wurde durch für jede Art verschiedene Variablen beeinflusst: In Teichrohrsängern (Acrocephalus scirpaceus) war die Prävalenz mit dem Alter assoziiert, in Seidensängern (Cetti cetti) mit der Jahreszeit und in Haussperlingen (Passer domesticus) variierte die Prävalenz von Jahr zu Jahr. Auf dieser relativ kleinräumigen Skala hatte das Gebiet keinen Einfluss auf die Prävalenz, in keiner der Arten. Der Effekt des Alters auf die Prävalenz in Teichrohrsängern kann damit erklärt werden, dass adulte Teichrohrsänger bereits in Afrika waren und dort Kontakt mit einer anderen Parasiten Fauna hatten, während Jungtiere noch nicht dieser diversen Umgebung ausgesetzt waren. Für residente Seidensänger dagegen kann eine geringere Verfügbarkeit von Nahrungsmitteln im Herbst und Winter der Grund sein warum hier die Prävalenz saisonal variiert, welche die Vögel schwacher und damit empfänglicher für Infektionen macht.