Impacts of selective logging on haemosporidian infection and physiological correlates in tropical birds

Tropical forest degradation affects host-parasite interactions, determining the probability of animals acquiring an infection. The activation of an immune response to fight off infections requires energy and other resources such as antioxidants which may be redirected from growth and reproduction. A key question is how selective logging—the most common form of tropical forest degradation—impacts the prevalence of avian haemosporidian infection and its correlated physiological responses (nutritional and oxidative status markers). We investigated the prevalence of Plasmodium, Haemoproteus, and Leucocytozoon parasites in 14 understorey bird species in lowland, logged and unlogged, old-growth forests of Borneo. Prevalences of infections were similar between selectively logged and unlogged forests. To explore nutritional and oxidative status effects of haemosporidian infections, we examined associations between infections and plasma proteins, plasma triglycerides, and multiple blood-based markers of oxidative status, testing for an impact of selective logging on those markers. Birds infected with Plasmodium showed higher levels of plasma proteins and non-enzymatic antioxidant capacity, and lower levels of plasma triglycerides and glutathione, compared with haemosporidian-free individuals. Conversely, birds infected with Haemoproteus showed no changes in nutritional or physiological markers compared with uninfected individuals. These results indicate higher metabolic and physiological costs of controlling Plasmodium infection, compared with Haemoproteus, possibly due to higher pathogenicity of Plasmodium. Selectively logged forests had no effect on the responses of birds to infection, suggesting that the environmental conditions of degraded forests do not appear to induce any appreciable physiological demands in parasitised birds.     

Habitat Fragmentation and Ecological Traits Influence the Prevalence of Avian Blood Parasites in a Tropical Rainforest Landscape

In the tropical rainforests of northern Australia, we investigated the effects of habitat fragmentation and ecological parameters on the prevalence of blood-borne parasites (Plasmodium and Haemoproteus) in bird communities. Using mist-nets on forest edges and interiors, we sampled bird communities across six study sites: 3 large fragments (20–85 ha) and 3 continuous-forest sites. From 335 mist-net captures, we recorded 28 bird species and screened 299 bird samples with PCR to amplify and detect target DNA. Of the 28 bird species sampled, 19 were infected with Plasmodium and/or Haemoproteus and 9 species were without infection. Over one third of screened birds (99 individuals) were positive for Haemoproteus and/or Plasmodium. In forest fragments, bird capture rates were significantly higher than in continuous forests, but bird species richness did not differ. Unexpectedly, we found that the prevalence of the dominant haemosporidian infection, Haemoproteus, was significantly higher in continuous forest than in habitat fragments. Further, we found that ecological traits such as diet, foraging height, habitat specialisation and distributional ranges were significantly associated with blood-borne infections.     

MHC‐I provides both quantitative resistance and susceptibility to blood parasites in blue tits in the wild

Major histocompatibility complex (MHC) genes are central for the adaptive immune response against parasites. Here, we investigated potential associations among MHC‐I alleles and blood parasite infections in a natural breeding population of a passerine bird, the blue tit Cyanistes caeruleus, in central Spain. We screened both infection status (presence/absence of infection) and infection intensity to the pathogenic blood parasites Haemoproteus and Leucocytozoon. Three MHC‐I alleles (UA104, UA108 and UA117) were associated with higher or lower infection intensities by Leucocytozoon. Interestingly, these associations were dependent on age and were found both among young and adult birds. No MHC alleles were associated with infection intensity by Haemoproteus parasites. In addition, no significant relationships were detected between infection status by Haemoproteus and Leucocytozoon infections and MHC alleles. The very high prevalence of these two parasites in our study population (79–100%) poses challenges to identify associations with infection status and also suggests that clearance of infections may be rare. In conclusion, associations between specific MHC‐I alleles and Leucocytozoon parasites were related to either high or low infection intensities, and hence increased susceptibility or resistance to infection.     

Migration distance does not predict blood parasitism in a migratory songbird

Migration can influence host–parasite dynamics in animals by increasing exposure to parasites, by reducing the energy available for immune defense, or by culling of infected individuals. These mechanisms have been demonstrated in several comparative analyses; however, few studies have investigated whether conspecific variation in migration distance may also be related to infection risk. Here, we ask whether autumn migration distance, inferred from stable hydrogen isotope analysis of summer‐grown feathers (δ²H_f) in Europe, correlates with blood parasite prevalence and intensity of infection for willow warblers (Phylloscopus trochilus) wintering in Zambia. We also investigated whether infection was correlated with individual condition (assessed via corticosterone, scaled mass index, and feather quality). We found that 43% of birds were infected with Haemoproteus palloris (lineage WW1). Using generalized linear models, we found no relationship between migration distance and either Haemoproteus infection prevalence or intensity. There was spatial variation in breeding ground origins of infected versus noninfected birds, with infected birds originating from more northern sites than noninfected birds, but this difference translated into only slightly longer estimated migration distances (~214 km) for infected birds. We found no relationship between body condition indices and Haemoproteus infection prevalence or intensity. Our results do not support any of the proposed mechanisms for migration effects on host–parasite dynamics and cautiously suggest that other factors may be more important for determining individual susceptibility to disease in migratory bird species.     

The drivers of avian‐haemosporidian prevalence in tropical lowland forests of New Guinea in three dimensions

Haemosporidians are among the most common parasites of birds and often negatively impact host fitness. A multitude of biotic and abiotic factors influence these associations, but the magnitude of these factors can differ by spatial scales (i.e., local, regional and global). Consequently, to better understand global and regional drivers of avian‐haemosporidian associations, it is key to investigate these associations at smaller (local) spatial scales. Thus, here, we explore the effect of abiotic variables (e.g., temperature, forest structure, and anthropogenic disturbances) on haemosporidian prevalence and host–parasite networks on a horizontal spatial scale, comparing four fragmented forests and five localities within a continuous forest in Papua New Guinea. Additionally, we investigate if prevalence and host–parasite networks differ between the canopy and the understory (vertical stratification) in one forest patch. We found that the majority of Haemosporidian infections were caused by the genus Haemoproteus and that avian‐haemosporidian networks were more specialized in continuous forests. At the community level, only forest greenness was negatively associated with Haemoproteus infections, while the effects of abiotic variables on parasite prevalence differed between bird species. Haemoproteus prevalence levels were significantly higher in the canopy, and an opposite trend was observed for Plasmodium. This implies that birds experience distinct parasite pressures depending on the stratum they inhabit, likely driven by vector community differences. These three‐dimensional spatial analyses of avian‐haemosporidians at horizontal and vertical scales suggest that the effect of abiotic variables on haemosporidian infections are species specific, so that factors influencing community‐level infections are primarily driven by host community composition.     

Effect of haemosporidian infections on host survival and recapture rate in the blue tit

Parasites are ubiquitous in the wild and by imposing fitness costs on their hosts they constitute an important selection factor. One of the most common parasites of wild birds are Plasmodium and Haemoproteus, protozoans inhabiting the blood, which cause avian malaria and malaria‐like disease, respectively. Although they are expected to cause negative effects in infected individuals, in many cases studies in natural populations failed to detect such effect. Using data from seven breeding seasons (2008–2014), we applied a multistate capture–mark–recapture approach to study the effect of infection with malaria and malaria‐like parasites, individual age and sex on the probability of survival and recapture rate in a small passerine, the blue tit Cyanistes caeruleus, inhabiting the island of Gotland, Sweden. We found no effect of infection on survival prospects. However, the recapture rate of infected individuals was higher than that of uninfected ones. Thus, while our data do not support the presence of infection costs in terms of host survival, it suggests that parasites from the genera Plasmodium and Haemoproteus may affect some aspects of host behaviour, which translates into biased estimation of infection frequency at the population level.     

Sex-biased,but not plumage color-based,prevalence of haemosporidian parasites in free-range chickens

Previous studies found a relationship between blood parasite infection and bird gender, with higher prevalence in males. Some studies also found a relationship between host plumage color and parasitic infection, while others did not. Here, we investigated the blood parasite prevalence in correlation with sex and plumage color in free-range chickens (Gallus gallus domesticus) in China. We analyzed a total of 297 blood samples, out of which 234 chickens tested positive for haemosporidian parasites, with 78.5% parasite prevalence. Out of 139 males, 118 tested positive with 84.8% parasite prevalence while 116 of 158 female samples tested positive (73.4%). Leucocytotozoon was the most frequent genus isolated (193 infected individuals /234 birds), followed by Plasmodium (41 infected individuals/234 birds), with no Haemoproteus parasites being detected. There were no significant differences in the body parameters and chicken color plumages with regards to the infection status. Our study indicated that blood parasite infection was significantly different between male and female chickens, with infection prevalent in males.     

Parasite Prevalence Corresponds to Host Life History in a Diverse Assemblage of Afrotropical Birds and Haemosporidian Parasites

Avian host life history traits have been hypothesized to predict rates of infection by haemosporidian parasites. Using molecular techniques, we tested this hypothesis for parasites from three haemosporidian genera (Plasmodium, Haemoproteus, and Leucocytozoon) collected from a diverse sampling of birds in northern Malawi. We found that host life history traits were significantly associated with parasitism rates by all three parasite genera. Nest type and nest location predicted infection probability for all three parasite genera, whereas flocking behavior is an important predictor of Plasmodium and Haemoproteus infection and habitat is an important predictor of Leucocytozoon infection. Parasite prevalence was 79.1% across all individuals sampled, higher than that reported for comparable studies from any other region of the world. Parasite diversity was also exceptionally high, with 248 parasite cytochrome b lineages identified from 152 host species. A large proportion of Plasmodium, Haemoproteus, and Leucocytozoon parasite DNA sequences identified in this study represent new, previously undocumented lineages (n = 201; 81% of total identified) based on BLAST queries against the avian malaria database, MalAvi.     

Insights on the taxonomy of Haemoproteus parasites infecting cracid birds

The Haemosporida order is a well-supported clade of heteroxenous parasites transmitted by dipteran insects and frequently found parasitizing wild birds. These parasites have already been reported in all zoogeographic regions of the world, except for Antarctica. One of the potential hosts of haemosporidians is the Cracidae family, which includes approximately 50 species, 22 of which are present in Brazil, classified within nine genera. Data on haemosporidian infecting individuals of the Cracidae family is scarce, with only three Haemoproteus species being recorded in this group of birds. We found Haemoproteus spp. infection in all Penelope obscura bronzina analyzed. Among the parasites found, we observed two lineages of Haemoproteus (PENOBS02 and PENOBS03), which were characterized by morphological, molecular and phylogenetic approaches. The morphological data on cracid haemosporidian parasites, together with our phylogenetic results, allows discussions on the taxonomy of the Haemoproteus parasites that infect birds of the Cracidae family.     

Parasitemia in PCR‐detected Plasmodium and Haemoproteus infections in birds

Most comparative studies of avian blood parasites based on visual inspection of smears have reported Haemoproteus infections to be more prevalent than Plasmodium infections in both tropical and temperate locations. Recently, molecular techniques have increased our ability to detect infections often missed on blood smears. Here we quantify the bias in prevalence resulting from unrecognized infections by examining blood smears of infected passerine birds from the West Indies (312 individuals) and the Ozark Mountains of southern Missouri (134 individuals) for which we could identify parasites based on cytochrome b sequences. In the West Indian sample, 63 of 179 Haemoproteus infections (35%) and 121 of 133 Plasmodium infections (91%) were not detected among ca. 2,800 red blood cells examined per smear. In the Missouri sample, 19 of 77 Haemoproteus infections (25%) and 31 of 57 Plasmodium infections (54%) were not detected among ca. 10,000 red blood cells examined. Clearly, visual inspection of blood smears at this level of effort fails to recognize many malaria parasite infections ascertained by PCR screening, and this bias for Plasmodium parasites exceeds that for Haemoproteus parasites. The lower prevalence of Plasmodium compared to Haemoproteus reported in comparative studies based on blood smears likely reflects differences in detection rather than infection rates. Estimates obtained from visual inspection of blood smears would appear to be more indicative of parasite virulence and how well host individuals control infections than of the prevalence of infections in host populations.     

Health impact of blood parasites in breeding great tits

Hypotheses of hemoparasite-mediated sexual selection and reproductive costs rely on the assumption that avian blood parasite infections are harmful to their hosts. To test the validity of this assumption, we examined the health impact of Haemoproteus blood parasites on their great tit (Parus major) host. We hypothesised that if blood parasites impose any serious health impact on their avian hosts, then infected individuals must differ from uninfected ones in respect to hemato-serological general health and immune parameters. A 3-year study of two great tit populations, breeding in contrasting (urban and rural) habitats in south-east Estonia, revealed that Haemoproteus blood parasites affected the health state of their avian hosts. Infected individuals had elevated lymphocyte hemoconcentration and plasma gamma-globulin levels, indicating that both cell-mediated and humoral immune response mechanisms are involved in host defence. The effect of parasites on cell-mediated immunity was both age- and sex-specific, as infection status affected peripheral blood lymphocyte counts only in males, and among these, the magnitude of response was greater in old individuals than yearlings. Heterophile hemoconcentration and plasma albumin levels were not affected by infection status, suggesting that blood stages of Haemoproteus infection do not cause a severe inflammatory response. Parasitism was not related to hematocrit values, indicating that Haemoproteus infection does not cause anemia. In two years, infected individuals were heavier than uninfected ones in the urban but not in the rural study area. This suggests, that under certain circumstances (possibly related to reproductive tactics), breeding great tits may avoid losing body mass in order to save resources for an anti-parasite immune response. Received: 16 February 1998 / Accepted: 22 May 1998     

The epidemiology underlying age‐related avian malaria infection in a long‐lived host: the mute swan Cygnus olor

Quantifying the factors that predict parasite outbreak and persistence is a major challenge for both applied and fundamental biology. Key to understanding parasite prevalence and disease outbreaks is determining at what age individuals show signs of infection, and whether or not they recover. Age‐dependent patterns of the infection of a host population by parasites can indicate among‐individual heterogeneities in their susceptibility to, or rate of recovery from, parasite infections. Here, we present a cross‐sectional study of avian malaria in a long‐lived bird species, the mute swan Cygnus olor, examining age‐related patterns of parasite prevalence and modelling patterns of infection and recovery. One‐hundred and fifteen swans, ranging from one to nineteen years old, were screened for infection with Plasmodium, Haemoproteus and Leucocytozoon parasites. Infections with three cytochrome‐b lineages of Haemoproteus were found (pooled prevalence 67%), namely WW1 (26%), which is common in passerine birds, and two new lineages closely related to WW1: MUTSW1 (25%) and MUTSW2 (16%). We found evidence for age‐related infection in one lineage, MUTSW1. Catalytic models examining patterns of infection and recovery in the population suggested that infections in this population were not life‐long – recovery of individuals was included in the best fitting models. These findings support the results of recent studies that suggest hosts can clear infections, although patterns of infection‐related mortality in older birds remain to be studied in more detail.     

Seasonal dynamics in mosquito abundance and temperature do not influence avian malaria prevalence in the Himalayan foothills

We examined seasonal prevalence in avian haemosporidians (Plasmodium and Haemoproteus) in migrant and resident birds in western Himalaya, India. We investigated how infection with haemosporidians in avian hosts is associated with temporal changes in temperature and mosquito abundance along with host abundance and life‐history traits (body mass). Using molecular methods for parasite detection and sequencing partial cytochrome b gene, 12 Plasmodium and 27 Haemoproteus lineages were isolated. Our 1‐year study from December 2008 to December 2009 in tropical Himalayan foothills revealed a lack of seasonal variation in Plasmodium spp. prevalence in birds despite a strong correlation between mosquito abundance and temperature. The probability of infection with Plasmodium decreased with increase in temperature. Total parasite prevalence and specifically Plasmodium prevalence showed an increase with average avian body mass. In addition, total prevalence exhibited a U‐shaped relationship with avian host abundance. There was no difference in prevalence of Plasmodium spp. or Haemoproteus spp. across altitudes; parasite prevalence in high‐altitude locations was mainly driven by the seasonal migrants. One Haemoproteus lineage showed cross‐species infections between migrant and resident birds. This is the first molecular study in the tropical Himalayan bird community that emphasizes the importance of studying seasonal variation in parasite prevalence. Our study provides a basis for further evolutionary study on the epidemiology of avian malaria and spread of disease across Himalayan bird communities, which may not have been exposed to vectors and parasites throughout the year, with consequential implications to the risk of infection to naïve resident birds in high altitude.     

Effects of blood parasite infections on spatiotemporal migration patterns and activity budgets in a long‐distance migratory passerine

How blood parasite infections influence the migration of hosts remains a lively debated issue as past studies found negative, positive, or no response to infections. This particularly applies to small birds, for which monitoring of detailed migration behavior over a whole annual cycle has been technically unachievable so far. Here, we investigate how bird migration is influenced by parasite infections. To this end, we tracked great reed warblers (Acrocephalus arundinaceus) with multisensor loggers, characterized general migration patterns as well as detailed flight bout durations, resting times and flight heights, and related these to the genus and intensity of their avian haemosporidian infections. We found migration distances to be shorter and the onset of autumn migration to be delayed with increasing intensity of blood parasite infection, in particular for birds with Plasmodium and mixed‐genus infections. Additionally, the durations of migratory flight bout were prolonged for infected compared to uninfected birds. But since severely infected birds and particularly birds with mixed‐genus infections had shorter resting times, initial delays seemed to be compensated for and the timing in other periods of the annual cycle was not compromised by infection. Overall, our multisensor logger approach revealed that avian blood parasites have mostly subtle effects on migratory performance and that effects can occur in specific periods of the year only.     

Malaria infection and feather growth rate predict reproductive success in house martins

Carry-over effects take place when events occurring in one season influence individual performance in a subsequent season. Blood parasites (e.g. Plasmodium and Haemoproteus) have strong negative effects on the body condition of their hosts and could slow the rate of feather growth on the wintering grounds. In turn, these winter moult costs could reduce reproductive success in the following breeding season. In house martins Delichon urbica captured and studied at a breeding site in Europe, we used ptilochronology to measure growth rate of tail feathers moulted on the winter range in Africa, and assessed infection status of blood parasites transmitted on the wintering grounds. We found a negative association between haemosporidian parasite infection status and inferred growth rate of tail feathers. A low feather growth rate and blood parasite infections were related to a delay in laying date in their European breeding quarters. In addition, clutch size and the number of fledglings were negatively related to a delayed laying date and blood parasite infection. These results stress the importance of blood parasites and feather growth rate as potentially mechanisms driving carry-over effects to explain fitness differences in wild populations of migratory birds.     

Avian Plasmodium in Culex and Ochlerotatus Mosquitoes from Southern Spain: Effects of Season and Host-Feeding Source on Parasite Dynamics

Haemosporidians, a group of vector-borne parasites that include Plasmodium, infect vertebrates including birds. Although mosquitoes are crucial elements in the transmission of avian malaria parasites, little is known of their ecology as vectors. We examined the presence of Plasmodium and Haemoproteus lineages in five mosquito species belonging to the genera Culex and Ochlerotatus to test for the effect of vector species, season and host-feeding source on the transmission dynamics of these pathogens. We analyzed 166 blood-fed individually and 5,579 unfed mosquitoes (grouped in 197 pools) from a locality in southern Spain. In all, 15 Plasmodium and two Haemoproteus lineages were identified on the basis of a fragment of 478 bp of the mitochondrial cytochrome b gene. Infection prevalence of blood parasites in unfed mosquitoes varied between species (range: 0–3.2%) and seasons. The feeding source was identified in 91 mosquitoes where 78% were identified as bird. We found that i) several Plasmodium lineages are shared among different Culex species and one Plasmodium lineage is shared between Culex and Ochlerotatus genera; ii) mosquitoes harboured Haemoproteus parasites; iii) pools of unfed females of mostly ornithophilic Culex species had a higher Plasmodium prevalence than the only mammophylic Culex species studied. However, the mammophylic Ochlerotatus caspius had in pool samples the greatest Plasmodium prevalence. This relative high prevalence may be determined by inter-specific differences in vector survival, susceptibility to infection but also the possibility that this species feeds on birds more frequently than previously thought. Finally, iv) infection rate of mosquitoes varies between seasons and reaches its maximum prevalence during autumn and minimum prevalence in spring.     

Phylogenetic relationships of haemosporidian parasites in New World Columbiformes, with emphasis on the endemic Galapagos dove

DNA-sequence analyses of avian haemosporidian parasites, primarily of passerine birds, have described the phylogenetic relationships of major groups of these parasites, which are in general agreement with morphological taxonomy. However, less attention has been paid to haemosporidian parasites of non-passerine birds despite morphological and DNA-sequence evidence for unique clades of parasites in these birds. Detection of haemosporidian parasites in the Galapagos archipelago has raised conservation concerns and prompted us to characterise the origins and diversity of these parasites in the Galapagos dove (Zenaida galapagoensis). We used partial mitochondrial cytochrome b (cyt b) and apicoplast caseinolytic protease C (ClpC) genes to develop a phylogenetic hypothesis of relationships of haemosporidian parasites infecting New World Columbiformes, paying special attention to those parasites infecting the endemic Galapagos dove. We identified a well-supported and diverse monophyletic clade of haemosporidian parasites unique to Columbiformes, which belong to the sub-genus Haemoproteus (Haemoproteus). This is a sister clade to all the Haemoproteus (Parahaemoproteus) and Plasmodium parasites so far identified from birds as well as the Plasmodium parasites of mammals and reptiles. Our data suggest that the diverse Haemoproteus parasites observed in Galapagos doves are not endemic to the archipelago and likely represent multiple recent introductions.     

Exo-erythrocytic development of two Haemoproteus species (Haemosporida,Haemoproteidae), with description of Haemoproteus dumbbellus,a new blood parasite of bunting birds (Emberizidae)

Avian haemosporidians are widespread parasites categorized into four families of the order Haemosporida (Apicomplexa). Species of the subgenus Parahaemoproteus (genus Haemoproteus) belong to the Haemoproteidae and are transmitted by Culicoides biting midges. Reports of death due to tissue damage during haemoproteosis in non-adapted birds have raised concerns about these pathogens, especially as their exo-erythrocytic development is known for only a few Haemoproteus spp. More research is needed to better understand the patterns of the parasites’ development in tissues and their impact on avian hosts. Yellowhammers Emberiza citrinella (Emberizidae) and common house martins Delichon urbicum (Hirundinidae) were screened for Haemoproteus parasites by microscopic examination of blood films and PCR-based testing. Individuals with single infection were selected for histological investigations. H & E-stained sections were screened for detection and characterization of the exo-erythrocytic stages, while chromogenic in situ hybridization (CISH) and phylogenetic analysis were performed to confirm the Haemoproteus origin and their phylogenetic relationships. Haemoproteus dumbbellus n. sp. was discovered in Emberiza citrinella single-infected with the lineage hEMCIR01. Meronts of H. dumbbellus n. sp. developed in various organs of five of six tested individuals, a pattern which was reported in other Haemoproteus species clustering in the same clade, suggesting this could be a phylogenetic trait. By contrast, in Delichon urbicum infected with the Haemoproteus lineage hDELURB2, which was linked to the more distantly related parasite Haemoproteus hirundinis, only megalomeronts were found in the pectoral muscles of two of six infected individuals. All exo-erythrocytic stages were confirmed to be Haemoproteus parasites by CISH using a Haemoproteus genus-specific probe. While the development of meronts seems to be typical for species of the clade containing H. dumbbellus, further investigations and data from more species are needed to explore whether a phylogenetic pattern occurs in meront or megalomeront formation.