Does avian malaria reduce fledging success: an experimental test of the selection hypothesis

Like many parasites, avian haematozoa are often found at lower infection intensities in older birds than young birds. One explanation, known as the “selection” hypothesis, is that infected young birds die before reaching adulthood, thus removing the highest infection intensities from the host population. We tested this hypothesis in the field by experimentally infecting nestling rock pigeons (Columba livia) with the malaria parasite Haemoproteus columbae. We compared the condition and fledging success of infected nestlings to that of uninfected controls. There was no significant difference in the body mass, fledging success, age at fledging, or post-fledging survival of experimental versus control birds. These results were unexpected, given that long-term studies of older pigeons have demonstrated chronic effects of H. columbae. We conclude that H. columbae has little impact on nestling pigeons, even when they are directly infected with the parasite. Our study provides no support for the selection hypothesis that older birds have lower parasite loads because parasites are removed from the population by infected nestlings dying. To our knowledge, this is the first study to test the impact of avian malaria using experimental inoculations under natural conditions.     

Endoparasites of black-bellied whistling ducks in southern Texas.

Endoparasites detected in the black-bellied whistling duck (Dendrocygnaautumnalis) include one nasal mite, four nematodes, three trematodes, five cestodes, and two acanthocephalans. Each of these represents a new host record. Overall, 47% of the birds were parasitized with an average of 12 helminths per infected bird. Helminths were significantly more common in juveniles than in adults; more females than males were parasitized, but the difference was not statistically significant. No correlation existed between the parasite load and the physical condition of the host. Tissue damage in infected birds was minimal and limited to nematode cysts in the proventriculi. Parasite loads were light, apparently reflecting the food habits of the host.     

Comparison of autumn and spring migration strategies of Neotropical migratory landbirds in northeast Belize

ABSTRACT Migration represents one of the most vulnerable stages of a migrant's life cycle, but the strategies and stopover sites used by Neotropical migrants in Central America are not well known. We carried out constant‐effort mist netting and conducted censuses along transects during one autumn (2007) and one spring (2008) migration in northeast Belize. We recorded more landbird migrant species in autumn (63) than in spring (54), and spring abundance was >25% lower for 88% of transient species. These differences in presence and abundance indicate that routes and stopover strategies vary between seasons and species. In autumn, fuel loads, calculated as any increase in mass above lean body mass (LBM), were generally small (mean = 5.9% LBM and 10.1% LBM for wintering and transient species, respectively) and fuel deposition rates and minimum stopover durations suggest that some individuals replenished energy reserves in our study area. Variation in autumn fuel loads meant that some individuals had reserves sufficient for flights >1000 km. Fuel loads were larger in spring for 16 of 17 species, and the mean spring fuel load for transient species (32.5% LBM) was sufficient for a flight from northeast Belize to North America without refueling. The similarity in spring passage times between northeast Belize and the Gulf Coast of the United States also suggests that energy reserves were not replenished in northeast Belize prior to crossing the Gulf of Mexico. We hypothesize that sufficient energy reserves are accumulated during spring stopovers in northern South America or elsewhere in Mesoamerica to allow migrants to fly directly to North America without refueling.     

Avian malaria infection intensity influences mosquito feeding patterns

Pathogen-induced host phenotypic changes are widespread phenomena that can dramatically influence host–vector interactions. Enhanced vector attraction to infected hosts has been reported in a variety of host–pathogen systems, and has given rise to the parasite manipulation hypothesis whereby pathogens may adaptively modify host phenotypes to increase transmission from host to host. However, host phenotypic changes do not always favour the transmission of pathogens, as random host choice, reduced host attractiveness and even host avoidance after infection have also been reported. Thus, the effects of hosts’ parasitic infections on vector feeding behaviour and on the likelihood of parasite transmission remain unclear. Here, we experimentally tested how host infection status and infection intensity with avian Plasmodium affect mosquito feeding patterns in house sparrows (Passer domesticus). In separate experiments, mosquitoes were allowed to bite pairs containing (i) one infected and one uninfected bird and (ii) two infected birds, one of which treated with the antimalarial drug, primaquine. We found that mosquitoes fed randomly when exposed to both infected and uninfected birds. However, when mosquitoes were exposed only to infected individuals, they preferred to bite the non-treated birds. These results suggest that the malarial parasite load rather than the infection itself plays a key role in mosquito attraction. Our findings partially support the parasite manipulation hypothesis, which probably operates via a reduction in defensive behaviour, and highlights the importance of considering parasite load in studies on host–vector–pathogen interactions.     

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.     

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.     

Increased Endoparasite Infection in Late-Arriving Individuals of a Trans-Saharan Passerine Migrant Bird

Earlier migration in males than in females is the commonest pattern in migrating passerines and is positively related to size dimorphism and dichromatism. The early arrival of males is a costly trait that may confer reproductive advantages in terms of better territories and/or mates. Given the physiological cost of migration, early migrants are those in best condition and accordingly the prevalence, load, and/or diversity of parasites is expected to increase in both sexes for late migrants. To test this hypothesis, we sampled 187 trans-Saharan migrant garden warblers Sylvia borin and 64 resident serins Serinus serinus (as a control for potential circannual patterns in parasite load) during spring migration in Spain. We assessed the prevalence of blood parasites (Haemoproteus, Plasmodium, and Leucocytozoon) and the prevalence and load of intestinal parasites (mainly coccidians and spirurids). The relationship between parasite (prevalence, load, and richness) and the timing of passage through a stopover area was tested using generalized linear models. Protandry occurs in the monomorphic garden warbler and males migrated on average 5.5 days before females. Intestinal parasite richness increased with the date of migration. The timing of migration was unrelated to the presence or load of the other parasite groups analyzed. Our results support the idea that the timing of migration is a condition-dependent trait and suggests that multiple intestinal parasite infestations could delay migration in birds. Even in monomorphic species parasites may play a role in sexual selection by delaying the arrival of the most infected individuals at breeding grounds, thereby further increasing the benefits of mating with early-arriving individuals.     

Different paths – the same virulence: experimental study on avian single and co-infections with Plasmodium relictum and Plasmodium elongatum

Co-infections are prevalent worldwide, however, we are still struggling to understand interactions between different parasites and their impacts on host fitness. In the present experimental study we analysed the infection dynamics of two avian malarial parasites Plasmodium elongatum (genetic lineage pERIRUB01) and Plasmodium relictum (genetic lineage pSGS1) and their impacts on host health during single and co-infections. We reveal that P. elongatum intensity of parasitemia is enhanced by the presence of P. relictum during co-infection, while the parasitemia of P. relictum stays the same. This illustrates how development of a parasite (P. elongatum) which infects both mature and young (polychromatic) red blood cells (RBCs) is facilitated during co-infection with a parasite which specialises in adult RBCs only (P. relictum). The virulence of co-infections was similar to that of the more virulent parasite (P. elongatum). However, the profile of infection and the mechanisms that caused mortality were different. Birds infected with P. elongatum only start to die due to non-regenerative anaemia, when intensity of parasitemia is light and the number of polychromatic RBCs decrease dramatically. Meanwhile, co-infected birds start to die when the mean intensity of parasitemia reaches 10% and the number of polychromatic RBCs increases abnormally, reflecting regenerative anaemia. Our findings reveal that typically measured parameters of virulence (e.g., mortality rate, level of hematocrit) can be the same during single and co-infections, but the mechanisms responsible for the observed virulence can be different. This information serves a better understanding of the processes underpinning the interactions of co-infected parasite species.     

When and where to fuel before crossing the Sahara desert – extended stopover and migratory fuelling in first-year garden warblers Sylvia borin

Large numbers of passerine migrants cross the Sahara desert every year on their way to-and-from wintering areas in tropical Africa. In the desert, hardly any fuelling opportunities exist and most migrants have to prepare in advance. A central question is how inexperienced birds know where to fuel. Inexperienced garden warblers Sylvia borin were studied in Greece just before the desert crossing in autumn. Body mass data collected at two sites indicate that most birds do not fuel for the desert crossing further north. For the first time, detailed information about stopover duration close to the Sahara desert was studied by using light weight radio-transmitters. Results from Crete show that most first-year garden warblers arrive with relatively small fuel loads in relation to lean body mass (<30%), stay for 13–20 d and depart with an average fuel load of about 100%. Radio-tagged birds performed small scale movements initially and took advantage of fig fruits. Birds trapped at fig trees were heavier than birds trapped with tape lures, showing that tape lures can bias the sample of migrants trapped. The precise fuelling pattern found indicates that first-year migrants must also include external spatial cues to make the preparation for crossing the desert in the right area.     

Partitioning average competition and extreme-genotype effects in genetically diverse infections

Competition between parasite genotypes in genetically diverse infections is widespread. However, experimental evidence on how genetic diversity influences total parasite load is variable. Here we use an additive partition equation to quantify the negative effect of inter-genotypic competition on total parasite load in diverse infections. Our approach controls for extreme-genotype effects, a process that can potentially neutralise, or even reverse, the negative effect of competition on total parasite load. A single extreme-genotype can have a disproportionate effect on total parasite load if it causes the highest parasite load in its single-infection, while increasing its performance in diverse relative to single infections. We show that in theory such disproportionate effects of extreme-genotypes can lead to a higher total parasite load in diverse infections than expected, even if competition reduces individual parasite performance on average. Controlling for the extreme-genotype effect is only possible if the competition effect on total parasite load is measured appropriately as the average difference between the realised number of each parasite genotype in mixed infections and the expected number based on single infection parasite loads. We apply this approach to sticklebacks that were experimentally infected with different trematode genotypes. On average, genetically diverse infections had lower parasite loads than expected from single-infection results. For the first time we demonstrate that competition between co-infecting genotypes per se caused the parasite load reduction, while extreme-genotype effects were not significant. We thus suggest that to correctly quantify the effect of competition alone on total parasite load in genetically diverse infections, the extreme-genotype effect has to be controlled for.     

Apoptosis of non-parasitised red blood cells in Plasmodium yoelii malaria

Recently, while studying erythrocytic apoptosis during Plasmodium yoelii infection, we observed an increase in the levels of non-parasitised red blood cell (nRBC) apoptosis, which could be related to malarial anaemia. Therefore, in the present study, we attempted to investigate whether nRBC apoptosis is associated with the peripheral RBC count, parasite load or immune response. To this end, BALB/c mice were infected with P. yoelii 17XL and nRBC apoptosis, number of peripheral RBCs, parasitaemia and plasmatic levels of cytokines, nitric oxide and anti-RBC antibodies were evaluated at the early and late stages of anaemia. The apoptosis of nRBCs increased at the late stage and was associated with parasitaemia, but not with the intensity of the immune response. The increased percentage of nRBC apoptosis that was observed when anaemia was accentuated was not related to a reduction in peripheral RBCs. We conclude that nRBC apoptosis in P. yoelii malaria appears to be induced in response to a high parasite load. Further studies on malaria models in which acute anaemia develops during low parasitaemia are needed to identify the potential pathogenic role of nRBC apoptosis.     

Parasites and Sexual Selection in Birds of Paradise

We studied blood parasite infections in relation to aspectsof sexual selection and mate choice in 10 species of birds ofparadise. Across species there was a significant, positive correlationbetween relative parasite intensity and showiness in males.Parasite infections also correlated across species with thedegree of sexual dimorphism and varied with mating systems.Promiscuous species were showier and had significantly higherparasite prevalences than monogamous species. Within one species,Lawes' Parotia (Parotia lawesii), parasite intensity was negativelycorrelated with all phenotypic traits examined, a pattern significantlydifferent than random. The mating success of males with lowparasite intensities varied, but males with high intensitiesdid not mate. Sampling of individual males on repeated occasionsrevealed large temporal differences in parasite counts whichspanned the range believed to affect behavior and mating success.Whereas the interspecific correlations support one predictionof the Hamilton and Zuk hypothesis on parasites and sexual selection,the intraspecific data are equivocal with respect to a secondprediction of this hypothesis. Parasites appear to influencethe behavior of Lawes' Parotia, but alternative explanationsto that of Hamilton and Zuk for this effect are equally plausibleand there is no evidence of a link between female choice andthe traits in males indicative of parasite loads. We suggestthat female Lawes' Parotia may be avoiding highly infected malesrather than actively choosing parasite-resistant males.     

Red blood cell motions in high-hematocrit blood flowing through a stenosed microchannel

We investigated the behavior of red blood cells (RBCs) in a microchannel with stenosis using a confocal micro-PTV system. Individual trajectories of RBCs in a concentrated suspension of up to 20% hematocrit (Hct) were measured successfully. Results indicated that the trajectories of healthy RBCs became asymmetric before and after the stenosis, while the trajectories of tracer particles in pure water were almost symmetric. The asymmetry was greater in 10% Hct than in 20% Hct. We also investigated the effect of deformability of RBCs on the cell-free layer thickness by hardening RBCs using a glutaraldehyde treatment. The results indicated that deformability is the key factor in the asymmetry of cell-free layer thickness. Therefore, the motions of RBCs are influenced strongly by the Hct, the deformability, and the channel geometry. These results give fundamental knowledge for a better understanding of blood flow in microcirculation and biomedical microdevices.     

A meta-analysis of parasite virulence in nestling birds

Parasitism is a common cause of host mortality, but little is known about the ecological factors affecting parasite virulence (the rate of mortality among infected hosts). We reviewed 117 field estimates of parasite-induced nestling mortality in birds, showing that there was significant consistency in mortality among host and parasite taxa. Virulence increased towards the tropics in analyses of both species-specific data and phylogenetic analyses. We found evidence of greater parasite prevalence being associated with reduced virulence. Furthermore, bird species breeding in open nest sites suffered from greater parasite-induced mortality than hole-nesting species. By contrast, parasite specialization and generation time of parasites relative to that of hosts explained little variation in virulence. Likewise, there were little or no significant effects of host genetic variability, host sociality, host migration, host insular distribution or host survival on parasite virulence. These findings suggest that parasite-induced nestling mortality in birds is mainly determined by geographical location and to a smaller extent nest site and prevalence.     

Speciation and diversification of parasite lineages: an analysis of congeneric parasite species in vertebrates

The evolutionary diversification of living organisms is a central research theme in evolutionary ecology, and yet it remains difficult to infer the action of evolutionary processes from patterns in the distribution of rates of diversification among related taxa. Using data from helminth parasite communities in 76 species of birds and 114 species of mammals, the influence of four factors that may either be associated with or modulate rates of parasite speciation were examined in a comparative analysis. Two measures of the relative number of congeneric parasite species per host species were used as indices of parasite diversification, and related to host body mass, host density, latitude, and whether the host is aquatic or terrestrial. The occurrence of congeneric parasites was not distributed randomly with respect to these factors. Aquatic bird species tended to harbour more congeneric parasites than terrestrial birds. Large-bodied mammal species, or those living at low latitudes, harboured more congeneric parasites than small-bodied mammals, or than those from higher latitudes. Host density had no apparent association with either measures of parasite diversification. These patterns, however, reflect only the present-day distribution of parasite diversification among host taxa, and not the evolutionary processes responsible for diversification, because the apparent effects of the factors investigated disappeared once corrections were made for host phylogeny. This indicates that features other than host body size, host density, latitude, and whether the habitat is terrestrial or aquatic, have been the key driving forces in the diversification of parasitic helminth lineages. This revised version was published online in July 2006 with corrections to the Cover Date.     

Circulation of parasites among fishes from lakes in the Caribou Mountains,Alberta, Canada

Circulation of 24 macroparasite species among 12 species of fish was evaluated within samples of hosts collected from 9 lakes on an isolated plateau in northern Alberta, Canada. Twenty-seven parasite taxa (24 species plus the larval stages of Triaenophorus crassus, T. stizostedionis, and Raphidascaris acus) had the potential to be circulated among hosts. Sixteen parasite taxa were recovered from a single host species within a lake. Of the 11 remaining nonspecialist taxa, 4 were larval stages that matured in fish or birds and 7 were adults. Eight of the 11 cases of circulation among hosts involved lake whitefish, and this host was involved in the transmission of 5 species to piscivorous fishes. Despite evidence for the circulation of 7 taxa among the 4 species of sympatric Salmonidae, 60-99% of all worms were recovered from just 1 species of host. These results indicated that approximately 60% of the parasite taxa that infected fish in these lakes were absolute host specialists. The remaining 40% of parasite taxa had restricted host ranges, with most examples of parasite circulation limited to the 2 species of sympatric coregonid.     

Rapid isolation of single malaria parasite-infected red blood cells by cell sorting

Malaria research often requires isolation of individually infected red blood cells (RBCs) or of a homogenous parasite population derived from a single parasite (clone). Traditionally, isolation of individual, parasitized RBCs or parasite cloning is achieved by limiting dilution or micromanipulation. This protocol describes a method for more efficient cloning of the malaria parasite; the method uses a cell sorter to rapidly isolate Plasmodium falciparum-infected RBCs singly. By gating the parameters of forward-angle light scatter and side-angle light scatter in a cell sorter, singly infected RBCs can be isolated and automatically deposited into a 96-well culture plate within 1 min. Including a Percoll purification step; the entire procedure to seed a 96-well plate with singly infected RBCs can take <40 min. This highly efficient single-cell sorting protocol should be useful for cloning of both laboratory parasite populations from genetic manipulation experiments and clinical samples.     

Blood parameter changes during stopover in a long-distance migratory shorebird, the bar-tailed godwit Limosa lapponica taymyrensis

Bar-tailed godwits migrate from West African wintering sites to breeding areas in northern Russia with only one stopover. We compared hematocrit (Hct), blood hemoglobin concentration (Hb), and mean cell hemoglobin concentration (MCHb; a measure of the relative proportion of Hb in the cellular blood fraction) between arriving godwits lured to land 60 km short of the stopover site and godwits during subsequent refueling. The Hct and Hb of arriving godwits was low when compared to that of refueling birds. On the stopover site, Hct and Hb correlated positively with size-corrected body mass. In addition, Hb and MCHb reached peak levels in the last days of stopover. We explored the possibility of regenerative anemia in arriving godwits by comparing the fraction of reticulocytes (young red blood cells) between arriving and refueling birds. No differences were found. Therefore, we suggest that the increase in Hct, Hb, and MCHb during refueling is not in response to a severe anemic state at arrival. Rather, we suggest that the increase in blood parameters may anticipate the increased aerobic requirements of impending migratory flight and possibly satisfy heightened oxygen demands of the larger body mass of fattened birds. The Hct increase on the stopover site may also serve to buffer the red blood cell population against possible red blood cell breakdown during long-distance flight.     

Aspects of the biology and parasitology of the speckled pigeon Columba guinea L. from Ahmadu Bello University Campus, Zaria, North Central State, Nigeria

The nesting activity, food, fat content and parasites of the speckled pigeon Columba guinea L. from Ahmadu Bello University at Zaria in Nigeria were studied during 1973. Five parasite species were found; the digenean trematode Echinostomum revolutum (Froelich), the cestodes Aporina delafondi (Raillet) and two species of Raillietina and the hippoboscid fly Pseudolynchia canariensis Macquart. The cestodes were the most important parasites since 92% of all birds examined were infected. Male birds had a heavier cestode load than female birds. The nesting season was essentially from October to April with a peak of activity during December and January. Male birds were heavier and showed greater variation in morphometric characteristics than females. Immature birds were lighter than adults but their wing and bill lengths were similar. These pigeons were mainly grain eating birds and the abundance of ground-nuts, guinea corn, rice and millet as items of food apparently coincided with the planting and harvesting seasons.
Pigeons in the nesting season had fewer fat deposits in the heart and smaller numbers of cestodes which were, however, heavier than those from pigeons in the non-nesting season. Male pigeons were lighter in the nesting season than males in the non-nesting season and had less fat but a greater parasite load in the nesting season than females.     

Differential Haemoparasite Intensity between Black Sparrowhawk (Accipiter melanoleucus) Morphs Suggests an Adaptive Function for Polymorphism

Recent research suggests that genes coding for melanin based colouration may have pleiotropic properties, in particular conveying raised immune function. Thus adaptive function of polymorphism may be associated with parasite resistance. The black sparrowhawk Accipiter melanoleucus is a polymorphic raptor with two morphs. Over most of its range the light morph is commonest, however within the recently colonised Western Cape of South Africa the dark morph predominates. The species breeds in winter throughout South Africa, however unlike in the rest of the species'' South African range, the Western Cape experiences a winter rainfall regime, where arthropod vectors which transmit haematozoan parasites may be more abundant. We hypothesise that the higher frequency of dark morph birds in this region may be due to their improved parasite resistance, which enables them to cope with higher parasite pressure. If so, we predict that dark morph black sparrowhawks would have lower parasite burdens than light morph birds. Within our population the prevalence of the two most common haematozoan parasites was high, with 72% of adults infected with Haemoproteus nisi and 59% of adults infected with Leucocytozoon toddi. We found no difference in prevalence for either parasite between adult morphs, or between chicks of different parental morphs. However, within adults infected with H. nisi, infection intensity was significantly higher in light morphs than dark morphs. This suggests that dark morphs have lower parasite loads than light morphs due to resistance rather than morph-specific habitat exploitation. Greater resistance to Haemoproteus parasites may therefore be one of the mechanisms through which dark morph black sparrowhawks have a selective advantage in this region and may explain why they are most common in our study area. In other regions, the cost to benefit ratio may be in favour of the light morph, where parasites are less abundant or virulent.