Beta diversity, prevalence, and specificity of avian haemosporidian parasites throughout the annual cycle of Chilean Elaenia (Elaenia chilensis), a Neotropical austral migrant.

Migratory birds are implicated in dispersing haemosporidian parasites over great geographic distances. However, their role in sharing these vector-transmitted blood parasites with resident avian host species along their migration flyway is not well understood. We studied avian haemosporidian parasites in 10 localities where Chilean Elaenia, a long-distance Neotropical austral migrant species, spends part of its annual cycle to determine local parasite transmission among resident sympatric host species in the elaenia's distributional range across South America. We sampled 371 Chilean Elaenias and 1,818 birds representing 243 additional sympatric species from Brazilian wintering grounds to Argentinian breeding grounds. The 23 haemosporidian lineages found in Chilean Elaenias exhibited considerable variation in distribution, specialization, and turnover across the 10 avian communities in South America. Parasite lineage dissimilarity increased with geographic distance, and infection probability by Parahaemoproteus decreased in localities harbouring a more diverse haemosporidian fauna. Furthermore, blood smears from migrating Chilean Elaenias and local resident avian host species did not contain infective stages of Leucocytozoon, suggesting that transmission did not take place in the Brazilian stopover site. Our analyses confirm that this Neotropical austral migrant connects avian host communities and transports haemosporidian parasites along its distributional range in South America. However, the lack of transmissive stages at stopover site and the infrequent parasite lineage sharing between migratory host populations and residents at breeding and wintering grounds suggest that Chilean Elaenias do not play a significant role in dispersing haemosporidian parasites, nor do they influence local transmission across South America.

Host foraging behavior and nest type influence prevalence of avian haemosporidian parasites in the Pantanal.

Avian haemosporidians from the genera Plasmodium and Haemoproteus are vector transmitted parasites. A growing body of evidence suggests that variation in their prevalence within avian communities is correlated with a variety of avian ecological traits. Here, we examine the relationship between infection probability and diversity of haemosporidian lineages and avian host ecological traits (average body mass, foraging stratum, migratory behavior, and nest type). We used molecular methods to detect haemosporidian parasites in blood samples from 642 individual birds of 149 species surveyed at four localities in the Brazilian Pantanal. Based on cytochrome b sequences, we recovered 28 lineages of Plasmodium and 17 of Haemoproteus from 31 infected avian species. Variation in lineage diversity among bird species was not explained by avian ecological traits. Prevalence was heterogenous across avian hosts. Bird species that forage near the ground were less likely to be infected by Haemoproteus, whereas birds that build open cup nests were more likely infected by Haemoproteus. Furthermore, birds foraging in multiple strata were more likely to be infected by Plasmodium. Two other ecological traits, often related to host resistance (body mass and migratory behavior), did not predict infection probability among birds sampled in the Pantanal. Our results suggest that avian host traits are less important determinants of haemosporidian diversity in Pantanal than in other regions, but reinforces that host attributes, related to vector exposure, are to some extent important in modulating infection probability within an avian host assemblage.

Low host specificity and lack of parasite avoidance by immature ticks in Brazilian birds.

Ticks are ectoparasites that feed on blood of a broad taxonomic range of terrestrial and flying vertebrates and are distributed across a wide range of environmental conditions. Here, we explore the biotic and abiotic factors on infestation probability of ticks of the genus Amblyomma and assess the degree of host specificity based on analysis of 1028 birds surveyed across Brazil. We show that tick infestation rates exhibited considerable variation across the 235 avian species analyzed and that the probability of an individual bird being parasitized by immature ticks (larvae and nymphs) increased with annual precipitation. Host phylogeny and two host ecological traits known to promote tick exposure (body mass and foraging behavior) did not predict infestation probability. Moreover, immature ticks displayed a low degree of host specificity at the family level. Lastly, tick occurrence in birds carrying infection with avian malaria and related parasites did not differ from those free of these haemosporidian parasites, indicating a lack of parasite avoidance by immature ticks. Our findings demonstrate that tick occurrence in birds across Brazilian biomes responds to environmental factors rather than ecological and evolutionary host attributes.

Host movement and time of year influence tick parasitism in Pantanal birds.

Ticks are among the best studied parasitic groups as they spread important pathogens of medical and veterinary importance worldwide. Migratory birds can play an important role in transporting ticks infected with pathogens across wide geographic regions. It is therefore important to understand which factors promote tick parasitism rates across their avian hosts and the associated potential for disease spread. Here, we identified the host attributes of infestation probability of ticks from the genus Amblyomma in 955 birds from Pantanal, Brazil. Infestation rates exhibited considerable variation across the 129 avian species surveyed and were explained by both host ecological traits and evolutionary history. The probability of an individual bird being infested with immature ticks (larvae and/or nymphs) was higher across resident bird species that forage at ground level and during the wet season. Bird species that feed on vertebrates were less likely to be infested by ticks. Other ecological traits known to promote tick exposure (age, body mass, social behavior, and sex) did not predict infestation probability. Our findings demonstrate that tick occurrence in Pantanal birds is determined by avian host attributes, but tick occurrence throughout the year constrains exposure to host-seeking ticks. Moreover, the ecology of the avian host might prevent the potential spread of tick-borne diseases outside Pantanal as migratory hosts are likely less infested by ticks.

Immature hard ticks infected with Rickettsia amblyommatis on breeding birds from Pantanal.

Immature hard ticks from the genus Amblyomma feed on blood from a wide range of Neotropical avian hosts. They serve as vectors for pathogens of medical and veterinary importance, such as Rickettsia agents of the spotted fever group (SFG). Hence, determining ecological factors that increase encounter rates between immature ticks and their avian hosts may contribute to the understanding of tick-borne diseases transmission. Here, we used 720 individual birds from 96 species surveyed in the Brazilian Pantanal to test whether host breeding season influenced tick infestation probabilities. Additionally, collected ticks were screened for Rickettsia agents to describe new avian-tick-bacteria associations. Our models revealed that the probability of an individual bird being infested with immature ticks was similar during the breeding and pre-breeding season, but higher loads of immature tick stages were found during the breeding season. Host sex did not predict infestation probability, but Rickettsia agents recovered from ticks were more prevalent during the pre-breeding season. The new records of host usage by larvae and nymphs of Amblyomma in Pantanal and the growing body of tick surveys in Neotropical avian communities, suggest that immature ticks may benefit from avian blood sources during their annual cycle. The low number of infected ticks with Rickettsia agents on Pantanal birds suggest that this vertebrate group are likely not acting as reservoirs for these microorganisms. However, long-term surveys at the same site are imperative to determine which tick species are acting as reservoirs for Rickettsia agents in Pantanal and determine whether birds are playing a role in dispersing ticks and tick-borne pathogens.

Higher infection probability of haemosporidian parasites in Blue-black Grassquits (Volatinia jacarina) inhabiting native vegetation across Brazil.

Human induced changes on landscape can alter the biotic and abiotic factors that influence the transmission of vector-borne parasites. To examine how infection rates of vector-transmitted parasites respond to changes on natural landscapes, we captured 330 Blue-black Grassquits (Volatinia jacarina) in Brazilian biomes and assessed the prevalence and diversity of avian haemosporidian parasites (Plasmodium and Haemoproteus) across avian host populations inhabiting environment under different disturbance and climatic conditions. Overall prevalence in Blue-black Grassquits was low (11%) and infection rates exhibited considerable spatial variation, ranging from zero to 39%. Based on genetic divergence of cytochrome b gene, we found two lineages of Haemoproteus (Parahaemoproteus) and 10 of Plasmodium. We showed that Blue-black Grassquit populations inhabiting sites with higher proportion of native vegetation cover were more infected across Brazil. Other landscape metrics (number of water bodies and distance to urban areas) and climatic condition (temperature and precipitation) known to influence vector activity and promote avian malaria transmission did not explain infection probability in Blue-black Grassquit populations. Moreover, breeding season did not explain prevalence across avian host populations. Our findings suggest that avian haemosporidian prevalence and diversity in Blue-black Grassquit populations are determined by recent anthropogenic changes in vegetation cover that may alter microclimate, thus influencing vector activity and parasite transmission.

Amblyomma ticks consumed by a giant cowbird, Molothrus oryzivorus.

The removal of ectoparasites is a common behavior found across animal taxa and is a determinant to avoid the negative effects of parasites' presence. Eventually, the elimination of ectoparasites is associated with mutualistic interactions. Cleaner birds remove ectoparasites, providing benefits to its mutualistic host by reducing parasite burden while they obtain a protein food source. Here we report some evidence that giant cowbirds (Molothrus oryzivorus) may have an important role as a cleaner bird. We found 74 adult ticks inside the ventriculus of one male giant cowbird. The ticks belonged to three different species: Amblyomma dubitatum, A. sculptum and A. triste. We found that the sex-ratio of the consumed adult ticks was not different from 1:1. Although additional data are necessary, the large number of ticks found suggests that the giant cowbird may have developed a mutualistic association with large, social mammals such as capybaras (Hydrochoerus hydrochaeris), since this animal is an important host species for the three tick species found in the present study.

The importance of novelty: male-female interactions among blue-black grassquits in captivity.

Mate choice is a primary mechanism driving the evolution of sexually selected traits such as elaborate displays and ornaments. In a majority of taxa studied to date, females are seen to actively sample and evaluate multiple males, presumably to optimize mating opportunities. During this process females may encounter males both familiar and novel, a distinction that might influence how mate choice proceeds. Using a socially monogamous passerine, the blue-black grassquit (Volatinia jacarina), we studied how females respond to novel versus familiar ("paired") males, and how encounters with novel males influence subsequent interactions with their paired males. Additionally, we measured the hormonal response of males after visualizing their paired females interacting with novel males. We found that females were attentive to novel males irrespective of these males' phenotypic attributes, suggesting that in these interactions novelty is highly relevant. After exposure to novel males, females tended to respond aggressively towards their paired males; by contrast, the behaviour of males towards their paired females did not change. Moreover, we did not detect any hormonal responses of males to viewing their paired females interacting with novel males. Together these results suggest that the distinction between familiarity and novelty may hold special relevance for females in mate choice, a finding that bears upon our understanding of the evolution of extra-pair paternity and reproductive behaviour.