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.     

Phylogenetic signals in host–parasite associations for Neotropical bats and Nearctic desert rodents

Hosts and their parasites have strong ecological and evolutionary relationships, with hosts representing habitats and resources for parasites. In the present study, we use approaches developed to evaluate the statistical dependence of species trait values on phylogenetic relationships to determine whether host–parasite relationships (i.e. parasite infections) are contingent on host phylogeny. If host–parasite relationships are contingent on the ability of hosts to provide habitat or resources to parasites, and if host phylogeny is an effective surrogate for among‐host variation in habitat and resource quality, host–parasite relationships should evince phylogenetic signals (i.e. be contingent on host phylogeny). Because the strength of ecological relationships between parasites and their hosts may affect the likelihood of phylogenetic signals occurring in host–parasite relationships, we hypothesized that (1) host specificity would be positively correlated with the strength of phylogenetic signals and (2) the strength of phylogenetic signals will be greater for parasites that rely more on their host throughout their life cycle. Analyses were conducted for ectoparasites from tropical bats and for ectoparasites, helminths, and coccidians from desert rodents. Phylogenetic signals were evaluated for parasite presence and for parasite prevalence. The frequency of phylogenetic signal occurrence was similar for parasite presence and prevalence, with a signal detected in 24–27% of cases at the species level and in 67% and 15% of cases at the genus level for parasites of bats and rodents, respectively. No differences in signal strength or the likelihood of detecting a signal existed between groups of parasites. Phylogenetic signal strength was correlated with host specificity, suggesting that mechanisms increasing host specificity also increase the likelihood of a phylogenetic signal in host use by parasites. Differences in the transmission mode did not affect signal strength or the likelihood of detecting a signal, indicating that variation in host switching opportunities associated with the transmission mode does not affect signal strength.     

Global warming will reshuffle the areas of high prevalence and richness of three genera of avian blood parasites

The importance of parasitism for host populations depends on local parasite richness and prevalence: usually host individuals face higher infection risk in areas where parasites are most diverse, and host dispersal to or from these areas may have fitness consequences. Knowing how parasites are and will be distributed in space and time (in a context of global change) is thus crucial from both an ecological and a biological conservation perspective. Nevertheless, most research articles focus just on elaborating models of parasite distribution instead of parasite diversity. We produced distribution models of the areas where haemosporidian parasites are currently highly diverse (both at community and at within‐host levels) and prevalent among Iberian populations of a model passerine host: the blackcap Sylvia atricapilla; and how these areas are expected to vary according to three scenarios of climate change. On the basis of these models, we analysed whether variation among populations in parasite richness or prevalence are expected to remain the same or change in the future, thereby reshuffling the geographic mosaic of host‐parasite interactions as we observe it today. Our models predict a rearrangement of areas of high prevalence and richness of parasites in the future, with Haemoproteus and Leucocytozoon parasites (today the most diverse genera in blackcaps) losing areas of high diversity and Plasmodium parasites (the most virulent ones) gaining them. Likewise, the prevalence of multiple infections and parasite infracommunity richness would be reduced. Importantly, differences among populations in the prevalence and richness of parasites are expected to decrease in the future, creating a more homogeneous parasitic landscape. This predicts an altered geographic mosaic of host‐parasite relationships, which will modify the interaction arena in which parasite virulence evolves.     

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.     

Priority effects within coinfected hosts can drive unexpected population‐scale patterns of parasite prevalence

Organisms are frequently coinfected by multiple parasite strains and species, and interactions between parasites within hosts are known to influence parasite prevalence and diversity, as well as epidemic timing. Importantly, interactions between coinfecting parasites can be affected by the order in which they infect hosts (i.e. within‐host priority effects). In this study, we use a single‐host, two‐pathogen, SI model with environmental transmission to explore how within‐host priority effects scale up to alter host population‐scale infection patterns. Specifically, we ask how parasite prevalence changes in the presence of different types of priority effects. We consider two scenarios without priority effects and four scenarios with priority effects where there is either an advantage or a disadvantage to being the first to infect in a coinfected host. Models without priority effects always predict negative relationships between the prevalences of both parasites. In contrast, models with priority effects can yield unimodal prevalence relationships where the prevalence of a focal parasite is minimized or maximized at intermediate prevalences of a coinfecting parasite. The mechanism behind this pattern is that as the prevalence of the coinfecting parasite increases, most infections of the focal parasite change from occurring as solo infections, to first arrival coinfections, to second arrival coinfections. The corresponding changes in parasite fitness as the focal parasite moves from one infection class to another then map to changes in focal parasite prevalence. Further, we found that even when parasites interact negatively within a host, they still can have positive prevalence relationships at the population scale. These results suggest that within‐host priority effects can change host population‐scale infection patterns in systematic (and initially counterintuitive) ways, and that taking them into account may improve disease forecasting in coinfected populations.     

Use of PCR for detection of subpatent infections of lizard malaria: implications for epizootiology

The estimated prevalence of a malaria parasite, Plasmodium mexicanum , of western fence lizards, Sceloporus occidentalis , was compared using two techniques: microscopic examination of blood smears, and nested PCR amplification of the 18S small subunit rRNA gene. Two sites in northern California, USA were investigated, one with known long-term high prevalence of the parasite (30% by blood smear scanning), and one with low prevalence (6%). The nested PCR readily detected very low-level infections (< 1 parasite per 10 000 erythrocytes); such infections are often subpatent by normal microscopic examination. False negatives (scored as not infected after scanning the blood smear, but found infected via PCR) were rare at both sites (4% at the high-prevalence site, 6% at the low-prevalence site). However, a greater proportion of infections was detected only by PCR at the low-prevalence site (50% vs. 9%). If 50% of the infections sustain very weak parasitaemia where lizards are rarely infected, this would accord with hypotheses that predict that parasites should reduce infection growth when transmission is uncommon. The study demonstrates that PCR is a powerful tool to detect very low-level malarial infections in vertebrate hosts, including those with nucleated erythrocytes.     

Geographical variation in blood parasites in feral pigeons: the role of vectors

Prevalence and intensity of blood parasites are known to vary in space within a same species, yet the causes underlying such variation are poorly known. Theoretically, blood parasites variation can be attributed to differences to exposure to parasite vectors and/or to differences in host susceptibility. Here, we show that prevalence of Haemoproteus columbae in feral pigeons Columba livia varied among five near-by populations (range 15%-100%), paralleled by variation in the abundance of its main vector, the louse flies Pseudolynchia canariensis. Geographic variation in intensity of blood parasites did not covary with abundance of vectors. Within populations, older individuals had a higher probability of being parasitized than younger ones, whereas younger birds, when infected, suffered higher intensities. Furthermore, we found no evidence of sex-related differences neither in prevalence nor in intensity of blood parasite infections. To demonstrate that geographical variation in prevalence was actually due to differences in vector exposure, we conducted two experiments based on translocation of unparasitized pigeons from a vector-free area to an area where both the parasite and vector were abundant. With the first experiment, we demonstrated that unparasitized pigeons were not resistant to the parasite because when transmission was possible pigeons became parasitized in a few months. With the second experiment, in which half of the pigeons were prevented from contacts with the vector, we ruled out the posibility that pigeons we considered as unparasitized would have suffered from latent infections. Therefore, both observational and experimental evidence supports the view that vector abundance is the major factor influencing the spatial variation in prevalence of H. columbae in pigeons.     

Spatiotemporal patterns of avian host–parasite interactions in the face of biogeographical range expansions

Exploration of interactions between hosts and parasitic symbionts is important for our understanding of the temporal and spatial distribution of organisms. For example, host colonization of new geographical regions may alter levels of infections and parasite specificity, and even allow hosts to escape from co‐evolved parasites, consequently shaping spatial distributions and community structure of both host and parasite. Here we investigate the effect of host colonization of new regions and the elevational distribution of host–parasite associations between birds and their vector‐transmitted haemosporidian blood parasites in two geological and geographical settings: mountains of New Guinea and the Canary Islands. Our results demonstrate that bird communities in younger regions have significantly lower levels of parasitism compared to those of older regions. Furthermore, host–parasite network analyses demonstrate that blood parasites may respond differently after arriving to a new region, through adaptations that allow for either expanding (Canary Islands) or retaining (New Guinea) their host niches. The spatial prevalence patterns along elevational gradients differed in the two regions, suggesting that region‐specific biotic (e.g., host community) and abiotic factors (e.g., temperature) govern prevalence patterns. Our findings suggest that the spatiotemporal range dynamics in host–parasite systems are driven by multiple factors, but that host and parasite community compositions and colonization histories are of particular importance.     

Low haemosporidian diversity and one key-host species in a bird malaria community on a mid-Atlantic island (São Miguel, Azores)

When host species colonize new areas, the parasite assemblage infecting the hosts might change, with some parasite species being lost and others newly acquired. These changes would likely lead to novel selective forces on both host and its parasites. We investigated the avian blood parasites in the passerine bird community on the mid-Atlantic island of S?o Miguel, Azores, a bird community originating from continental Europe. The presence of haemosporidian blood parasites belonging to the genera Haemoproteus, Plasmodium, and Leucocytozoon was assessed using polymerase chain reaction. We found two Plasmodium lineages and two Leucocytozoon lineages in 11 bird species (84% of all breeding passerine species) on the island. These lineages were unevenly distributed across bird species. The Eurasian Blackbird (Turdus merula) was the key-host species (total parasite prevalence of 57%), harboring the main proportion of parasite infections. Except for Eurasian Blackbirds, all bird species had significantly lower prevalence and parasite diversity compared to their continental populations. We propose that in evolutionary novel bird communities, single species may act as key hosts by harboring the main part of the parasite fauna from which parasites "leak" into the other species. This would create very different host-parasite associations in areas recently colonized by hosts as compared to in their source populations.     

Interspecific differences in hematozoan infection in Sonoran desert Aimophila sparrows

Numerous studies have identified factors that control avian hematozoan infections, but the mechanisms that account for host differences in parasitemia remain largely speculative. To address this issue, we compared the prevalence of these parasites in stained blood smears from four conspecific Sonoran desert Aimophila sparrow species sampled during their breeding season: rufous-winged (Aimophila carpalis; RWSP), rufous-crowned (Aimophila ruficeps; RCSP), Cassin's (Aimophila cassinii, CASP), and Botteri's (Aimophila botterii; BOSP) sparrows. Blood smears contained Haemoproteus fringillae (RWSP), Trypanosoma everetti (RWSP, RCSP, BOSP), Trypanosoma avium (CASP), and microfilariae (all species). Most (92.5%) RWSP (n=40) were infected with Haemoproteus, but this parasite was not detected in RCSP (n=20) or BOSP (n=20) and was found only in one (2.5%) CASP (n=40). Trypanosoma spp. and microfilariae were detected in all species, but prevalence differed between these four sparrow species. Species differences in parasite prevalence were not due to difference in sex, age, adult body mass, incubation period, breeding habitat, or plumage colorfulness. However, differences in Haemoproteus sp. prevalence correlated with preferred nesting height, as RWSP generally nest above ground, whereas the other species nest on or close to the ground. Elevated H. fringillae prevalence in breeding-condition RWSP presumably does not result from a seasonal relapse associated with breeding or require new infection because 1) this prevalence did not differ in males sampled during and outside (n=21) the breeding season, and 2) all male RWSP (n=25) that we held in captivity and shielded from new infections and influence of natural photoperiod for 1 yr had viable blood H. fringillae gametocytes. H. fringillae prevalence in fall-sampled hatch-year male RWSP (n=11) was 63.6%, demonstrating that this parasite can be transmitted on the breeding grounds and during the first months of life. T. everetti prevalence in RWSP was lower in winter than in summer and also in long-term captive than in free-ranging adults. Presence of this parasite in the blood of breeding males may depend on recrudescence of existing infections or new infections.     

Clonal diversity of a lizard malaria parasite, Plasmodium mexicanum, in its vertebrate host, the western fence lizard: role of variation in transmission intensity over time and space

Within the vertebrate host, infections of a malaria parasite (Plasmodium) could include a single genotype of cells (single-clone infections) or two to several genotypes (multiclone infections). Clonal diversity of infection plays an important role in the biology of the parasite, including its life history, virulence, and transmission. We determined the clonal diversity of Plasmodium mexicanum, a lizard malaria parasite at a study region in northern California, using variable microsatellite markers, the first such study for any malaria parasite of lizards or birds (the most common hosts for Plasmodium species). Multiclonal infections are common (50-88% of infections among samples), and measures of genetic diversity for the metapopulation (expected heterozygosity, number of alleles per locus, allele length variation, and effective population size) all indicated a substantial overall genetic diversity. Comparing years with high prevalence (1996-1998 = 25-32% lizards infected), and years with low prevalence (2001-2005 = 6-12%) found fewer alleles in samples taken from the low-prevalence years, but no reduction in overall diversity (H = 0.64-0.90 among loci). In most cases, rare alleles appeared to be lost as prevalence declined. For sites chronically experiencing low transmission intensity (prevalence approximately 1%), overall diversity was also high (H = 0.79-0.91), but there were fewer multiclonal infections. Theory predicts an apparent excess in expected heterozygosity follows a genetic bottleneck. Evidence for such a distortion in genetic diversity was observed after the drop in parasite prevalence under the infinite alleles mutation model but not for the stepwise mutation model. The results are similar to those reported for the human malaria parasite, Plasmodium falciparum, worldwide, and support the conclusion that malaria parasites maintain high genetic diversity in host populations despite the potential for loss in alleles during the transmission cycle or during periods/locations when transmission intensity is low.     

Parasites of lake sturgeon, Acipenser fulvescens (Chondrostei: Acipenseridae), from central Canada

Nineteen species of parasites were recovered from lake sturgeon, Acipenser fulvescens, from four major waterways of Central Canada; the Saskatchewan, Nelson, Winnipeg and Rainy River systems, Twelve of these are new host records. Host specific parasites, Crepidostomum auriculatum , Diclybothrium armatum , Spinitectus acipenseri and Truttaedacnitis clitellarius , forming the core parasite species, were recovered with the highest prevalence (≥70%) and were most widely distributed. Polypodium hydriforme was recovered from only stage IV sturgeon oocytes. With the exception of Pomphorhynchus bulbocolli , prevalence and intensity of endohelminth infections were not correlated with sex or age of host but the distribution of non host-specific parasites among sampling sites was determined by the type and relative abundance of food items consumed. The parasites of lake sturgeon are closely correlated to its diet and the species of parasites recovered are more similar to those of freshwater sturgeon in Eurasia than to other species of Acipenser in North America. The present parasite community of lake sturgeon appears to have been shaped by three major factors; the presence of core parasite species which predates geographic isolation, a benthic freshwater diet which has reshaped the parasite community to one comprising freshwater species and a long association with freshwater habitats which is reflected in the reproductive isolation of the lake sturgeon and lastly, the establishment of a host-specific parasite, Spinitectus acipenseri .     

Prevalence patterns of avian haemosporida on Hispaniola

We used PCR to screen for the presence of haemosporidian parasites (Phylum: Apicomplexa; Order: Haemosporida) in avian blood samples, and sequenced the parasite mitochondrial cytochrome b gene from infected hosts, to study patterns in the prevalence of haemosporidians in 1,166 individuals of 50 species in four habitats along an elevation gradient in the Sierra de Bahoruco, Dominican Republic, island of Hispaniola. We found an overall prevalence of 0.44 among species with ≥10 individuals sampled per year, but this varied considerably among species. We found no difference in infection rates between years, between males and females, between second‐year (<1 y old) and older birds, or among members of different foraging guilds. Prevalence differed significantly among migratory, endemic resident, and non‐endemic resident species, with endemics having the highest rates of infection. Prevalence also varied among habitats, decreasing with increasing elevation, but the pattern was confounded by variation in the host species present at each elevation. From 215 sequenced parasites from 17 species of avian hosts, we recovered multiple examples of 12 lineages of Haemoproteus (Parahaemoproteus), two lineages of a Columbiformes‐specific clade of H. (Haemoproteus), and 10 lineages of Plasmodium, with an additional seven lineages sampled only once. A single parasite lineage was responsible for 34.4% of all infections, but five more lineages made up 41.8% of all infections. Several lineages were broadly distributed across multiple host species, but six lineages, all H. (Haemoproteus) or H. (Parahaemoproteus), were recorded from at least five individuals of a single host, suggesting host specialization. The number of host species from which each parasite lineage was recovered varied from one to nine; several host species harbored as many as 5–9 parasite lineages. Longitudinal data suggest that while hosts might harbor the same parasite lineage for more than a year, some hosts appear to clear infections from their circulating blood, while others manifested infections by a different parasite lineage.     

Distribution anomalies in avian haemosporidian parasites in the southern Lesser Antilles

We compared the haemosporidian parasite faunas (Plasmodium and Haemoproteus) of small land birds on the islands of St Lucia, St Vincent and Grenada in the southern Lesser Antilles. The islands differ in distance from the South American source of colonists, proximity to each other, and similarity of their avifaunas. On each island, we obtained 419–572 blood samples from 22–25 of the 34–41 resident species. We detected parasite infection by PCR and identified parasite lineages by sequencing a portion of the mitochondrial cytochrome b gene. Parasite prevalence varied from 31% on St Lucia to 22% on St Vincent and 18% on Grenada. Abundant parasite lineages differed between the three islands in spite of the similarity in host species. As in other studies, the geographic distributions of the individual parasite lineages varied widely between local endemism and broad distribution within the West Indies, including cases of long‐distance disjunction. St Vincent was unusual in the near absence of Plasmodium parasites, which accorded with low numbers of suitable mosquito vectors reported from the island. Parasites on St Vincent also tended to be host specialists compared to those on St Lucia and Grenada. Similarity in parasite assemblages among the three islands varied in parallel with host assemblage similarity (but not similarity of infected hosts) and with geographic proximity. Parasite prevalence increased with host abundance on both St Lucia and St Vincent, but not on Grenada; prevalence did not vary between endemic and more widespread host species. In addition, the endemic host species harbored parasites that were recovered from a variety of non‐endemic species as well. These results support the individualistic nature of haemosporidian parasite assemblages in evolutionarily independent host populations.     

Ecological factors influencing disease risk in Eagle Owls Bubo bubo

In this study we assessed whether local habitat features and host population density influenced disease risk in Eagle Owl Bubo bubo fledglings. Measures of immune defence (concentrations of circulating white blood cells), prevalence of three parasite types (a blood parasite Leucocytozoon ziemanni , an insect Carnus haemapterus , and a tick Rhipicephalus sp.) and total number of parasite species were used to quantify disease risk. We tested the hypotheses that disease risk in fledglings was higher in nests located in areas with higher length of and proximity to watercourses (as a higher abundance and viability of parasites and vectors occur in wetter areas), higher cover of forest (as forest moistness and humidity can favour higher vector and parasite proliferation), higher habitat diversity (as environmental heterogeneity increases the pool of potential vectors and parasites) and higher local owl population density (as disease transmission might be density-dependent). The clearest relationship was with the proximity of freshwater, although the other hypotheses were also partially supported. Concentrations of white blood cells, the number of parasite species and, weakly, the prevalence of Carnus haemapterus were all higher in nests closer to watercourses. The prevalence of blood parasites increased with the cover of forested areas. Fledglings from nests located in more diverse habitats had higher white blood cell concentrations and showed higher prevalence of blood parasites. Finally, local host population density was positively correlated with the prevalence of blood parasites. The results suggest the existence of complex and interrelated links between ecological parameters and three different measures of disease risk, and highlight the importance of immunological approaches to assess disease risk at an intraspecific level.     

Epizootiology of blood parasites in an Australian lizard: a mark-recapture study of a natural population

The dynamics of a naturally endemic blood parasite (Hepatozoon hinuliae) were studied in a lizard (Eulamprus quoyii) host population, using 2 years of longitudinal data. We investigated how parasite abundance in the population varied over time, examined whether certain host sub-populations were more prone to infection, and compared parasite loads in relation to host reproductive behaviour. We recorded blood parasite infections of 331 individuals, obtained in 593 captures. Prevalence (the proportion of the host population infected) of blood parasites was high; approximately 66% of the lizard population was infected. Probability of infection increased with host age and size, but did not differ between the sexes. Within individuals, parasite load (the intensity of infection within individuals) did not vary over time, and was independent of host reproductive behaviour. Parasite load was significantly higher in males compared to females.     

A comparative study of the parasites in two populations of white-tailed deer

The study compares parasite prevalence in two geographically separated populations of white-tailed deer in central Pennsylvania. Differences in prevalence were found for certain of the parasites studied. Characteristics of curves comparing prevalence with host-age group, however, were remarkably similar for individual parasites from both populations. Prevalence increased with host age for certain species of parasite and decreased or remained constant for others. Some of the underlying biological properties of the infections which may be responsible for the characteristics of the age specific prevalence curves are discussed.     

Effects of spatial and host variables on hematozoa in white-crowned sparrows wintering in Baja California.

A survey of blood parasites was conducted in February 1995 on white-crowned sparrows (Zonotrichia leucophrys) wintering in two environmentally different localities of Baja California Sur (Mexico). Blood parasite prevalence was higher in La Purísima (49%) than in San José del Cabo (8%), but there were no differences between ages or sexes within each locality. All haematozoa infections were by Haemoproteus coatneyi, except one bird in each site that were positive for Trypanosoma sp. We found no evidence for the predicted negative relationship between host body condition and intensity of parasitism. The relatively high prevalence in one site suggests that an increase of hematozoa transmission may occur in that area.     

Association between haematozoan infections and reproduction in the Pied Flycatcher

1. Parasites may affect breeding success of their host since they compete for the same resources as their hosts. Reproduction may also increase the susceptibility of a host to parasite infections owing to lowered resistance to parasites during breeding.
2. We studied the association between breeding performance and haematozoan parasite infection in the Pied Flycatcher ( Ficedula hypoleuca ) by using both natural data on reproduction and data from clutch size manipulations.
3. The most frequent blood parasites of the Pied Flycatcher in central Finland were Haemoproteus pallidus , Haemoproteus balmorali and Trypanosoma avium complex.
4. We did not find evidence that these haematozoan parasites have any debilitating effects on either reproduction or survival. The variation in reproductive effort did not seem to influence susceptibility to new blood parasite infections.
5. The intensity of Haemoproteus balmorali tended to increase in infected males as the brood size was artificially enlarged. Also, in females intensity of H. pallidus infection tended to increase with the level of clutch size manipulation. Thus, increased reproductive effort seems to debilitate the ability of Pied Flycatcher to control chronic infections.
6. Individuals with enlarged clutches/broods increased their reproductive effort at the expense of defence towards parasites. The cost of current reproduction may then be at least partly mediated by haematozoan infections.