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The relationships between host phylogenetics, functional traits and parasites in wildlife remain poorly understood in the Neotropics, especially in habitats with marked seasonal variation. Here, we examined the effect of seasonality and host functional traits on the prevalence of avian haemosporidians ( Plasmodium and Haemoproteus ) in the Brazilian Caatinga, a seasonally dry tropical forest. 933 birds were evaluated for haemosporidian infections. We found a high parasitism prevalence (51.2%), which was correlated with phylogenetic relatedness among avian species. Prevalence varied drastically among the 20 well-sampled species, ranging from 0 to 70%. Seasonality was the main factor associated with infections, but how this abiotic condition influenced parasite prevalence varied according to the host-parasite system. Plasmodium prevalence increased during the rainy season and, after excluding the large sample size of Columbiformes ( n = 462/933), Plasmodium infection rate was maintained high in the wet season and showed a negative association with host body mass. No association was found between non-Columbiform bird prevalence and seasonality or body mass when evaluating both Plasmodium and Haemoproteus or only Haemoproteus infections. Parasite community was composed of 32 lineages including 7 new lineages. We evidenced that even dry domains can harbour a high prevalence and diversity of vector-borne parasites and pointed out seasonality as a ruling factor.

Host phylogenetic relatedness and ecological similarity are thought to contribute to parasite community assembly and infection rates. However, recent landscape level anthropogenic changes may disrupt host-parasite systems by impacting functional and phylogenetic diversity of host communities. We examined whether changes in host functional and phylogenetic diversity, forest cover, and minimum temperature influence the prevalence, diversity, and distributions of avian haemosporidian parasites (genera Haemoproteus and Plasmodium) across 18 avian communities in the Atlantic Forest. To explore spatial patterns in avian haemosporidian prevalence and taxonomic and phylogenetic diversity, we surveyed 2241 individuals belonging to 233 avian species across a deforestation gradient. Mean prevalence and parasite diversity varied considerably across avian communities and parasites responded differently to host attributes and anthropogenic changes. Avian malaria prevalence (termed herein as an infection caused by Plasmodium parasites) was higher in deforested sites, and both Plasmodium prevalence and taxonomic diversity were negatively related to host functional diversity. Increased diversity of avian hosts increased local taxonomic diversity of Plasmodium lineages but decreased phylogenetic diversity of this parasite genus. Temperature and host phylogenetic diversity did not influence prevalence and diversity of haemosporidian parasites. Variation in the diversity of avian host traits that promote parasite encounter and vector exposure (host functional diversity) partially explained the variation in avian malaria prevalence and diversity. Recent anthropogenic landscape transformation (reduced proportion of native forest cover) had a major influence on avian malaria occurrence across the Atlantic Forest. This suggests that, for Plasmodium, host phylogenetic diversity was not a biotic filter to parasite transmission as prevalence was largely explained by host ecological attributes and recent anthropogenic factors. Our results demonstrate that, similar to human malaria and other vector-transmitted pathogens, prevalence of avian malaria parasites will likely increase with deforestation., (Copyright © 2021 Australian Society for Parasitology. Published by Elsevier Ltd. All rights reserved.)

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., (Copyright © 2020 Elsevier B.V. All rights reserved.)

This study reports the case of a Manx shearwater (Puffinus puffinus) that died from avian malaria while under care at a rehabilitation center in Espírito Santo, Brazil. The bird was rescued on October 2018, and remained under care until it died suddenly on January 2019. A blood smear produced 8 days before death was negative for parasites, whereas a blood smear produced post-mortem revealed a high parasitemia by a parasite resembling Plasmodium cathemerium. The sequence of a 412 bp segment of the cyt-b gene was identical to that of lineage PADOM09, and phylogenetic analysis corroborated that this parasite was closely-related to known lineages of P. cathemerium. The acuteness and severity of the infection documented in this case suggest that seabirds of the order Procellariiformes might be highly susceptible to Plasmodium infections, raising the concern that avian malaria may present a significant threat to their conservation., Competing Interests: Declaration of competing interest The authors declare that they have no conflict of interest., (Copyright © 2020 Elsevier B.V. All rights reserved.)

The genus Plasmodium (Plasmodiidae) ranks among the most widespread intracellular protozoan parasites affecting a wide range of mammals, birds, and reptiles. Little information is available about lizard malaria parasites in South America, and the pathological features of the resulting parasitoses remain unknown or poorly understood. To partially fill in these gaps, we conducted blood smear analysis, molecular detection, and phylogenetic and pathological investigations in lizards inhabiting an Atlantic Forest fragment in Paraiba, Brazil. From 104 striped forest whiptails (Kentropyx calcarata) screened for the presence of haemosporidian parasites, 67 (64.4%) were positive. Four of five Amazon lava lizards (Strobilurus torquatus) we collected from this same area were also positive. A total of 27 forest whiptails were infected with a new genetic lineage of Plasmodium kentropyxi and other Plasmodium lineages were also detected. Histopathological analysis in infected forest whiptails revealed systemic intraerythrocytic Plasmodium stages, mainly gametocytes, in the liver, lung, and heart. Also, the liver of infected lizards had mild to moderate levels of Kupffer cell and melanomacrophage hypertrophy/hyperplasia with sinusoid leukocytosis. Overall, our findings suggest that an endemic Plasmodium species causes histological alterations that are not related to major pathological processes in striped forest whiptails.

The use of a sensitive and accurate parasite detection methodology is crucial in studies exploring prevalence of parasites in host populations or communities, and uncertainty in identifying parasite genera and/or lineages may limit the understanding of host-parasite interactions. Here, we used a multistate occupancy approach that accounts for imperfect detection to assess whether sex and breeding season influenced the prevalence of a specific Haemoproteus lineage (TARUF02) in a white-lined tanager population. Likewise, we explored whether the probability of detecting the target parasite in an infected bird using PCR and sequencing analyses may be influenced by season and host sex. We found little evidence that sex influenced the probability of an individual host being infected by a haemosporidian parasite. Conversely, we found that the probability of infection by Haemoproteus TARUF02 was ~30% higher during the breeding season, reflecting a higher prevalence of this parasite in this season. The probability that PCR detects DNA of haemosporidian parasite was higher for female birds, suggesting that they are more prone to be parasitized with parasitemia levels that are more successfully detected by molecular analysis. Sequencing successfully determined the Haemoproteus TARUF02 lineage in 60% of samples collected during the breeding season and 84% of samples collected during the non-breeding season. Understanding the ecology of hosts and aspects of their physiology that may influence the parasite infection is essential to better understanding of hemoparasite infections and how parasites influence their native hosts, through decreasing reproductive success, lifespan, and/or survival.

Avian malaria is a mosquito-borne disease caused by Plasmodium spp. protozoa, and penguins are considered particularly susceptible to this disease, developing rapid outbreaks with potentially high mortality. We report on an outbreak of avian malaria in Magellanic penguins (Spheniscus magellanicus) at a rehabilitation center in Espírito Santo, southeast Brazil. In August and September 2015, a total of 89 Magellanic penguins (87 juveniles and 2 adults) received care at Institute of Research and Rehabilitation of Marine Animals. Over a period of 2 weeks, Plasmodium infections were identified in eight individuals (9.0%), four of which died (mortality = 4.5%, lethality = 50%). Blood smears and sequencing of the mitochondrial cytochrome b gene revealed the presence of Plasmodium lutzi SPMAG06, Plasmodium elongatum GRW06, Plasmodium sp. PHPAT01, Plasmodium sp. SPMAG10, and Plasmodium cathemerium (sequencing not successful). Two unusual morphological features were observed in individuals infected with lineage SPMAG06: (a) lack of clumping of pigment granules and (b) presence of circulating exoerythrocytic meronts. Hematological results (packed cell volume, plasma total solids, complete blood cell counts) of positive individuals showed differences from those of negative individuals depending on the lineages, but there was no overarching pattern consistently observed for all Plasmodium spp. The epidemiology of the outbreak and the phylogeography of the parasite lineages detected in this study support the notion that malarial infections in penguins undergoing rehabilitation in Brazil are the result of the spillover inoculation by plasmodia that circulate in the local avifauna, especially Passeriformes.

Haemosporidian parasites of the genus Haemoproteus are widespread and can cause disease and even mortality in birds under natural and captive conditions. The Black-fronted Piping-guan (Aburria jacutinga) is an endangered Neotropical bird of the Cracidae (Galliformes) going through a reintroduction program to avoid extinction. We used microscopic examination and partial cytochrome b DNA sequencing to describe a new Haemoproteus species infecting Black-fronted Piping-guans bred and raised in captivity that were reintroduced into the Atlantic rainforest. Haemoproteus (Parahaemoproteus) paraortalidum n. sp. was detected in the blood of 19 out of 29 examined birds. The new species is distinguished from other haemoproteids due to the shape of gametocytes, which have pointed ends in young stages, and due to the presence of vacuole-like unstained spaces in macrogametocytes and numerous volutin granules both in macro- and microgametocytes. Illustrations of the new species are provided. Phylogenetic inference positioned this parasite in the Parahaemoproteus subgenus clade together with the other two Haemoproteus genetic lineages detected in cracids up to date. We discuss possible implications of the reintroduction of birds infected with haemosporidian parasites into the wild. Treatment of Haemoproteus infections remains insufficiently studied, but should be considered for infected birds before reintroduction to improve host reproductive and survival rates after release., (Copyright © 2018 Elsevier B.V. All rights reserved.)

Habitat modification may facilitate the emergence of novel pathogens, and the expansion of agricultural frontiers make domestic animals important sources of pathogen spillover to wild animals. We demonstrate for the first time that Plasmodium juxtanucleare, a widespread parasite from domestic chickens, naturally infects free-living passerines. We sampled 68 wild birds within and at the border of conservation units in central Brazil composed by Cerrado, a highly threatened biome. Seven out of 10 passerines captured in the limits of a protected area with a small farm were infected by P. juxtanucleare as was confirmed by sequencing a fragment of the parasite's cytochrome b. Blood smears from these positive passerines presented trophozoites, meronts and gametocytes compatible with P. juxtanucleare, meaning these birds are competent hosts for this parasite. After these intriguing results, we sampled 30 backyard chickens managed at the area where P. juxtanucleare-infected passerines were captured, revealing one chicken infected by the same parasite lineage. We sequenced the almost complete mitochondrial genome from all positive passerines, revealing that Brazilian and Asian parasites are closely related. P. juxtanucleare can be lethal to non-domestic hosts under captive and rehabilitation conditions, suggesting that this novel spillover may pose a real threat to wild birds.

We report, for the first time, the presence of ungulate malaria parasites in South America. We conducted PCR-based surveys of blood samples of multiple deer species and water buffalo from Brazil and detected Plasmodium sequences from pampas deer ( Ozotoceros bezoarticus ) samples. Phylogenic analysis revealed that the obtained sequences are closely related to the Plasmodium odocoilei clade 2 sequence from North American white-tailed deer ( Odocoileus virginianus ). Nucleotide differences suggest that malaria parasites in South American pampas deer and North American P. odocoilei clade 2 branched more recently than the Great American Interchange.

Habitat modification may change vertebrate and vector-borne disease distributions. However, natural forest regeneration through secondary succession may mitigate these effects. Here we tested the hypothesis that secondary succession influences the distribution of birds and their haemosporidian parasites (genera Plasmodium and Haemoproteus) in a seasonally dry tropical forest, a globally threatened ecosystem, in Brazil. Moreover, we assessed seasonal fluctuations in parasite prevalence and distribution. We sampled birds in four different successional stages at the peak and end of the rainy season, as well as in the middle and at the end of the dry season. A non-metric multidimensional scaling analysis revealed that bird communities in the pasture (i.e., highly modified) areas were different from those in the early, intermediate, and late successional areas (secondary forests). Among 461 individual birds, haemosporidian prevalence was higher in pasture areas than in the more advanced successional stages, but parasite communities were homogeneous across these areas. Parasite prevalence was higher in pasture-specialists birds (resilient species) than in forest-specialists species, suggesting that pasture-specialists may increase infection risk for co-occurring hosts. We found an increase in prevalence between the middle and end of the dry season, a period associated with the beginning of the breeding season (early spring) in southeastern Brazil. We also found effects of seasonality in the relative prevalence of specific parasite lineages. Our results show that natural forest recovery through secondary succession in SDTFs is associated with compositional differences in avian communities, and that advanced successional stages are associated with lower prevalence of avian haemosporidian parasites.

Background: Considerable success in reducing malaria incidence and mortality has been achieved in Brazil, leading to discussions over the possibility of moving towards elimination. However, more than reporting and counting clinical cases, elimination will require the use of efficient tools and strategies for measuring transmission dynamics and detecting the infectious reservoir as the primary indicators of interest for surveillance and evaluation. Because acquisition and maintenance of anti-malarial antibodies depend on parasite exposure, seroprevalence rates could be used as a reliable tool for assessing malaria endemicity and an adjunct measure for monitoring transmission in a rapid and cost-effective manner., Methods: This systematic review synthesizes the existing literature on seroprevalence of malaria in the Brazilian Amazon Basin. Different study designs (cross-sectional surveys and longitudinal studies) with reported serological results in well-defined Brazilian populations were considered. Medline (via PubMed), EMBASE and LILACS databases were screened and the articles were included per established selection criteria. Data extraction was performed by two authors and a modified critical appraisal tool was applied to assess the quality and completeness of cross-sectional studies regarding defined variables of interest., Results: From 220 single records identified, 23 studies were included in this systematic review for the qualitative synthesis. Five studies reported serology results on Plasmodium falciparum, 14 papers assessed Plasmodium vivax and four articles reported results on both Plasmodium species. Considerable heterogeneity among the evaluated malarial antigens, including sporozoite and blood stage antigens, was observed. The majority of recent studies analysed IgG responses against P. vivax antigens reflecting the species distribution pattern in Brazil over the last decades. Most of the published papers were cross-sectional surveys (73.9%) and only six cohort studies were included in this review. Three studies pointed to an association between antibodies against circumsporozoite protein of both P. falciparum and P. vivax and malaria exposure. Furthermore, five out 13 cross-sectional studies evidenced a positive association between IgG antibodies to the conserved 19-kDa C-terminal region of the merozoite surface protein 1 of P. vivax (PvMSP1 19 ) and malaria exposure., Conclusions: This systematic review identifies potential biomarkers of P. falciparum and P. vivax exposure in areas with variable and unstable malaria transmission in Brazil. However, this study highlights the need for standardization of further studies to provide an ideal monitoring tool to evaluate trends in malaria transmission and the effectiveness of malaria intervention programmes in Brazil. Moreover, the score-based weighted tool developed and used in this study still requires further validation.

Background: Haemosporidian parasites of the genera Plasmodium and Haemoproteus can have detrimental effects on individual birds and populations. Despite recent investigations into the distribution and richness of these parasites and their vertebrate hosts, little is known about their dipteran vectors. The Neotropics has the highest diversity of mosquitoes in the world, but few studies have tried to identify vectors in this area, hampering the understanding of the ecology of avian malaria in the highly diverse Neotropical environments., Methods: Shannon traps and active collection were used to capture 27,110 mosquitoes in a Seasonally Dry Tropical Forest in southeastern Brazil, a highly endangered ecosystem., Results: We screened 17,619 mosquito abdomens from 12 different species and several unidentified specimens of Culex, grouped into 1,913 pools, for the presence of haemosporidians. Two pools (out of 459) of the mosquito Mansonia titillans and one pool (out of 29) of Mansonia pseudotitillans were positive for Plasmodium parasites, with the detection of a new parasite lineage in the former species. Detected Plasmodium lineages were distributed in three different clades within the phylogenetic tree revealing that Mansonia mosquitoes are potential vectors of genetically distant parasites. Two pools of Culex spp. (out of 43) were positive for Plasmodium gallinaceum and closely related lineages. We found a higher abundance of these putative vectors in pasture areas, but they were also distributed in areas at intermediate and late successional stages. One pool of the mosquito Psorophora discrucians (out of 173) was positive for Haemoproteus., Conclusions: The occurrence of different Plasmodium lineages in Mansonia mosquitoes indicates that this genus encompasses potential vectors of avian malaria parasites in Brazil, even though we did not find positive thoraces among the samples tested. Additional evidence is required to assign the role of Mansonia mosquitoes in avian malaria transmission and further studies will add information about evolutionary and ecological aspects of avian haemosporidia and untangle the diversity of their vectors in Brazil.

We report two cases of lethal avian malaria in Magellanic Penguins (Spheniscus magellanicus) captive at San Clemente del Tuyú, Argentina, approximately 560 km north of Argentinean breeding colonies of Magellanic Penguins. Blood smears revealed both penguins were concurrently infected by Plasmodium (Haemamoeba) tejerai, Plasmodium (Huffia) sp., and Plasmodium (Novyella) sp.

One of the unresolved issues in the ecology of parasites is the relationship between host specificity and performance. Previous studies tested this relationship in different systems and obtained all possible outcomes. This led to the proposal of two hypotheses to explain conflicting results: the trade-off and resource breadth hypotheses, which are treated as mutually exclusive in the literature and were corroborated by different studies. In the present study, we used an extensive database on avian malaria from Brazil and combined analyses based on specificity indices and network theory, in order to test which of those hypotheses might best explain our model system. Contrary to our expectations, there was no correlation between specificity and prevalence, which contradicts both hypotheses. In addition, we detected a strong modular structure in our host-parasite network and found that its modules were not composed of geographically close, but of phylogenetically close, host species. Based on our results, we reached the conclusion that trade-off and resource breadth hypotheses are not really mutually exclusive. As a conceptual solution we propose "The Integrative Hypothesis of Parasite Specialization", a novel theoretical model that explains the contradictory results found in our study and reported to date in the literature., (Copyright © 2015 Australian Society for Parasitology Inc. Published by Elsevier Ltd. All rights reserved.)

Blood parasites are potential threats to the health of penguins and to their conservation and management. Little penguins Eudyptula minor are native to Australia and New Zealand, and are susceptible to piroplasmids (Babesia), hemosporidians (Haemoproteus, Leucocytozoon, Plasmodium) and kinetoplastids (Trypanosoma). We studied a total of 263 wild little penguins at 20 sites along the Australian southeastern coast, in addition to 16 captive-bred little penguins. Babesia sp. was identified in seven wild little penguins, with positive individuals recorded in New South Wales, Victoria and Tasmania. True prevalence was estimated between 3.4% and 4.5%. Only round forms of the parasite were observed, and gene sequencing confirmed the identity of the parasite and demonstrated it is closely related to Babesia poelea from boobies (Sula spp.) and B. uriae from murres (Uria aalge). None of the Babesia-positive penguins presented signs of disease, confirming earlier suggestions that chronic infections by these parasites are not substantially problematic to otherwise healthy little penguins. We searched also for kinetoplastids, and despite targeted sampling of little penguins near the location where Trypanosoma eudyptulae was originally reported, this parasite was not detected.

The pathogenesis of malaria is complex, generating a broad spectrum of clinical manifestations. One of the major complications and concerns in malaria is anemia, which is responsible for considerable morbidity in the developing world, especially in children and pregnant women. Despite its enormous health importance, the immunological mechanisms involved in malaria-induced anemia remain incompletely understood. Plasmodium vivax, one of the causative agents of human malaria, is known to induce a strong inflammatory response with a robust production of immune effectors, including cytokines and antibodies. Therefore, it is possible that the extent of the immune response not only may facilitate the parasite killing but also may provoke severe illness, including anemia. In this review, we consider potential immune effectors and their possible involvement in generating this clinical outcome during P. vivax infections., (Copyright © 2014, American Society for Microbiology. All Rights Reserved.)

Avian malaria is a mosquito-borne disease caused by Plasmodium spp. Avian plasmodia are recognized conservation-threatening pathogens due to their potential to cause severe epizootics when introduced to bird populations with which they did not co-evolve. Penguins are considered particularly susceptible, as outbreaks in captive populations will often lead to high morbidity and rapid mortality. We used a multidisciplinary approach to investigate an outbreak of avian malaria in 28 Magellanic penguins (Spheniscus magellanicus) at a rehabilitation center during summer 2009 in Florianópolis, Brazil. Hemosporidian infections were identified by microscopic and molecular characterization in 64% (18/28) of the penguins, including Plasmodium (Haemamoeba) tejerai, Plasmodium (Huffia) elongatum, a Plasmodium (Haemamoeba) sp. lineage closely related to Plasmodium cathemerium, and a Haemoproteus (Parahaemoproteus) sp. lineage closely related to Haemoproteus syrnii. P. tejerai played a predominant role in the studied outbreak and was identified in 72% (13/18) of the hemosporidian-infected penguins, and in 89% (8/9) of the penguins that died, suggesting that this is a highly pathogenic parasite for penguins; a detailed description of tissue meronts and lesions is provided. Mixed infections were identified in three penguins, and involved P. elongatum and either P. tejerai or P. (Haemamoeba) sp. that were compatible with P. tejerai but could not be confirmed. In total, 32% (9/28) penguins died over the course of 16 days despite oral treatment with chloroquine followed by sulfadiazine-trimethoprim. Hemosporidian infections were considered likely to have occurred during rehabilitation, probably from mosquitoes infected while feeding on local native birds, whereas penguin-mosquito-penguin transmission may have played a role in later stages of the outbreak. Considering the seasonality of the infection, rehabilitation centers would benefit from narrowing their efforts to prevent avian malaria outbreaks to the penguins that are maintained throughout summer.

The pathogens Plasmodium juxtanucleare and chicken anaemia virus (CAV) are easily transmitted and potentially harmful to chickens. In this study, we established an experimental model to investigate the effects of avian malaria caused by P. juxtanucleare in white leghorn specific-pathogen-free (SPF) chicks previously immunosuppressed with CAV. Parasitaemia, haematological variables and clinical and pathological parameters were determined in four different experimental groups: chicks coinfected by CAV and P. juxtanucleare strain (Coinfected group), chicks exclusively infected by CAV (CAV group) or P. juxtanucleare (Malaria group) and uninfected chicks (Control group). Our data demonstrated that P. juxtanucleare parasitaemia was significantly higher in the Coinfected group. Furthermore, haematological parameters, including the RBC, haematocrit and haemoglobin concentration were significantly reduced in coinfected chicks. In agreement with the changes observed in haematological features, the mortality among coinfected chicks was higher compared with animals with single infections. Clinical analysis indicated moderate changes related to different organs size (bursa of Fabricius, heart and liver) in coinfected birds. The experimental coinfection of SPF chickens with P. juxtanucleare and CAV may represent a research tool for the study of avian malaria after CAV immunosuppression, enabling measurement of the impacts caused by different pathogens during malarial infection.

Habitat alteration can disrupt host-parasite interactions and lead to the emergence of new diseases in wild populations. The cerrado habitat of Brazil is being fragmented and degraded rapidly by agriculture and urbanization. We screened 676 wild birds from three habitats (intact cerrado, disturbed cerrado and transition area Amazonian rainforest-cerrado) for the presence of haemosporidian parasites (Plasmodium and Haemoproteus) to determine whether different habitats were associated with differences in the prevalence and diversity of infectious diseases in natural populations. Twenty one mitochondrial lineages, including 11 from Plasmodium and 10 from Haemoproteus were identified. Neither prevalence nor diversity of infections by Plasmodium spp. or Haemoproteus spp. differed significantly among the three habitats. However, 15 of the parasite lineages had not been previously described and might be restricted to these habitats or to the region. Six haemosporidian lineages previously known from other regions, particularly the Caribbean Basin, comprised 50-80% of the infections in each of the samples, indicating a regional relationship between parasite distribution and abundance.