Plasmodium Relictum Research Articles

Relationship between avian malaria distribution and an exotic invasive mosquito in New Zealand

Although the mosquito vector responsible for the epizootic outbreaks of avian malaria in Hawaiian avifauna, Culex quinquefasciatus, has spread rapidly in New Zealand over the past three decades, no survey for malarial parasites has been conducted for more than 50 years. Avian malaria often causes extreme morbidity and mortality in novel hosts, and much of New Zealand's native avifauna has likely had no prior exposure, so the impact of this spread on native biodiversity is potentially serious. Wild non‐native birds were surveyed for malarial parasites at multiple locations, to test the hypothesis that the prevalence of malarial infection is associated positively with the known distribution of C. quinquefasciatus. Blood samples collected were analysed using a Polymerase Chain Reaction (PCR) assay. There was a strong pattern of decreasing percentage of samples positive for the blood parasite PCR marker from north to south, closely matching the known distribution of C. quinquefasciatus. A subsample of 10 PCR products were sequenced, and all identified as the malarial parasite Plasmodium relictum. Since historical surveys found no malarial parasites in the New Zealand avifauna, with a few minor exceptions, this suggests that this invasive exotic vector may be one factor driving the emergence of avian malaria. Sampling of wild non‐native birds at Orana Park, Christchurch, where a disease outbreak occurred recently in a captive native bird population, suggested that such outbreaks may spill‐back into local wild bird populations. The high prevalence of malarial infection observed in certain non‐native species, particularly blackbirds, indicates that they may act as reservoirs of infection to native species.

EFFECTS OF CHRONIC AVIAN MALARIA (PLASMODIUM RELICTUM) INFECTION ON REPRODUCTIVE SUCCESS OF HAWAII AMAKIHI (HEMIGNATHUS VIRENS)

Abstract We studied the effects of chronic avian malaria (Plasmodium relictum) infections on the reproductive success of a native Hawaiian honeycreeper, Hawaii Amakihi (Hemignathus virens). Chronic malaria infections in male and female parents did not significantly reduce reproductive success as measured by clutch size, hatching success, fledging mass, number of nestlings fledged, nesting success (daily survival rate), and minimum fledgling survival. In fact, nesting success of pairs with chronically infected males was significantly higher than those with uninfected males (76% vs. 38%), and offspring that had at least one parent that had survived the acute phase of malaria infection had a significantly greater chance of being resighted the following year (25% vs. 10%). The reproduction and survival of infected birds were sufficient for a per-capita population growth rate >1, which suggests that chronically infected Hawaii Amakihi could support a growing population. Efectos de las Infecciones Cronicas de M...

DISTRIBUTION AND PREVALENCE OF MOSQUITO-BORNE DISEASES IN O’AHU ’ELEPAIO

Abstract ABSTRACT The endemic Hawaiian avifauna is one of the most imperiled on earth, and diseases have been one of the most serious causes of species declines. From 1995–2005, we mist-netted and banded 266 endangered O’ahu ’Elepaio (Chasiempis sandwichensis ibidis) from 27 sites, examined them for visible symptoms of avian pox virus (Poxvirus avium), and screened blood samples for avian malaria (Plasmodium relictum). Pox-like lesions and malaria were found in all ’Elepaio populations on O’ahu; no parts of the island were free of these mosquito-borne diseases. Each year, 20% ± 4% of ’Elepaio had active lesions likely caused by pox and an additional 16% ± 4% had deformities and missing toes indicative of healed pox lesions. Prevalence of malaria was 87% over all years combined. Pox prevalence varied among years and was associated with annual rainfall, presumably due to greater abundance of mosquito breeding sites in wet years. Rainfall amounts at least as high as those associated with pox epizootics in 19...

Parasites affect song complexity and neural development in a songbird

There is now considerable evidence that female choice drives the evolution of song complexity in many songbird species. However, the underlying basis for such choice remains controversial. The developmental stress hypothesis suggests that early developmental conditions can mediate adult song complexity by perturbing investment in the underlying brain nuclei during their initial growth. Here, we show that adult male canaries (Serinus canaria), infected with malaria (Plasmodium relictum) as juveniles, develop simpler songs as adults compared to uninfected individuals, and exhibit reduced development of the high vocal centre (HVC) song nucleus in the brain. Our results show how developmental stress not only affects the expression of a sexually selected male trait, but also the structure of the underlying song control pathway in the brain, providing a direct link between brain and behaviour. This novel experimental evidence tests both proximate and ultimate reasons for the evolution of complex songs and supports the Hamilton-Zuk hypothesis of parasite-mediated sexual selection. Together, these results propose how developmental costs may help to explain the evolution of honest advertising in the complex songs of birds.

COMPARATIVE SUSCEPTIBILITY OF INTRODUCED FOREST-DWELLING MOSQUITOES IN HAWAI'I TO AVIAN MALARIA, PLASMODIUM RELICTUM

To identify potential vectors of avian malaria in Hawaiian native forests, the innate susceptibility of Aedes albopictus, Wyeomyia mitchellii, and Culex quinquefasciatus from 3 geographical sites along an altitudinal gradient was evaluated using local isolates of Plasmodium relictum. Mosquitoes were dissected 5-8 and 9-13 days postinfective blood meal and microscopically examined for oocysts and salivary-gland sporozoites. Sporogony was completed in all 3 species, but prevalence between species varied significantly. Oocysts were detected in 1-2% and sporozoites in 1-7% of Aedes albopictus that fed on infected ducklings. Wyeomyia mitchellii was slightly more susceptible, with 7-19% and 7% infected with oocysts and sporozoites, respectively. In both species, the median oocyst number was 5 or below. This is only the second Wyeomyia species reported to support development of a malarial parasite. Conversely, Culex quinquefasciatus from all 3 sites proved very susceptible. Prevalence of oocysts and sporozoites consistently exceeded 70%, regardless of gametocytemia or origin of the P. relictum isolate. In trials for which a maximum 200 oocysts were recorded, the median number of oocysts ranged from 144 to 200. It was concluded that Culex quinquefasciatus is the primary vector of avian malaria in Hawai'i.

Intracellular Hematozoa of Raptors: A Review and Update

The intracellular hematozoa of vertebrates are apicomplexan parasites with a life cycle consisting of 3 major phases: schizogony (asexual), gametogony (sexual), and sporogony (asexual). Most members have heteroxenous life cycles, wherein gametogony and sporogony occur in an arthropod vector and schizogony occurs in the vertebrate host. Leucocytozoon toddi occurs in Falconiformes and Leucocytozoon ziemanni in Strigiformes. Considered nonpathogenic in adult raptors, Leucocytozoon can cause mortality in nestlings. Haemoproteus is generally considered nonpathogenic in raptors; however, there are recent reports of fatalities in owls. Plasmodium is the true malarial parasite of birds and mammals. One species, Plasmodium relictum, is considered pathogenic for raptors. Atoxoplasma (previously Lankesterella) is an avian coccidian with both blood and intestinal stages. Babesia has been reported in raptors and might cause anemia and blindness in young falcons. In this article, advances in hematozoon diagnosis, treatment, and prevention are discussed. Although some hematozoa of raptors are considered nonpathogenic, high parasitemias in peripheral blood could indicate an underlying disease process.

High prevalence of blood parasites in hawfinch Coccothraustes coccothraustes

Fifty-seven hawfinches Coccothraustes coccothraustes were caught in May–June 1982–2001 on the Curonian Spit in the Baltic Sea and investigated by microscopical examination of stained blood films. Haemoproteus fringillae, H. tartakovskyi, Leucocytozoon dubreuili, L. fringillinarum, L. majoris, Plasmodium relictum, P. vaughani, Trypanosoma avium, T. everetti, and microfilariae were identified. The overall prevalence of infection was 100%. Prevalences of Haemoproteus spp. (89.5%), Plasmodium spp. (61.4%), Leucocytozoon spp. (78.9%), Trypanosoma spp. (26.3%), and microfilariae (29.8%) were recorded. No differences were discernible in parasite fauna, prevalence, or intensity of infection between males and females or between young and adult birds. The majority of infections (86.0% of all birds) were mixed, with parasites from two to five different genera present in each blood smear. These birds were failed breeders migrating through the Curonian Spit. It is probable that heavy haematozoan infections can influence the breeding success of birds.

Detection of avian malaria (Plasmodium spp.) in native land birds of American Samoa

This study documents the presence ofPlasmodium spp. in landbirds ofcentral Polynesia. Blood samples collectedfrom eight native and introduced species fromthe island of Tutuila, American Samoa wereevaluated for the presence of Plasmodiumspp. by nested rDNA PCR, serology and/ormicroscopy. A total of 111/188 birds (59%)screened by nested PCR were positive. Detection of Plasmodium spp. was verifiedby nucleotide sequence comparisons of partial18S ribosomal RNA and TRAP(thrombospondin-related anonymous protein)genes using phylogenetic analyses. All samplesscreened by immunoblot to detect antibodiesthat cross-react with Hawaiian isolates of Plasmodium relictum (153) were negative. Lack of cross-reactivity is probably due toantigenic differences between the Hawaiian andSamoan Plasmodium isolates. Similarly,all samples examined by microscopy (214) werenegative. The fact that malaria is present,but not detectable by blood smear evaluation isconsistent with low peripheral parasitemiacharacteristic of chronic infections. Highprevalence of apparently chronic infections,the relative stability of the native land birdcommunities, and the presence of mosquitovectors which are considered endemic andcapable of transmitting avian Plasmodia,suggest that these parasites are indigenous toSamoa and have a long coevolutionary historywith their hosts.

Blood Parasites of American Crows (Corvus brachyrhynchos) and Fish Crows (Corvus ossifragus) in Florida, U.S.A.

Blood films from 46 fish crows (Corvus ossifragus Wilson) and 42 American crows (Corvus brachyrhynchos Brehm) from Florida, U.S.A., were examined for blood parasites. Haemoproteus picae Coatney and Roudabush, Haemoproteus danilewskii Kruse, Trypanosoma avium (Danilewsky), and microfilariae of an unidentified filarioid were identified from both species of crows. An unidentified species of Haemoproteus and Trypanosoma ontarioensis Woo and Bartlett were observed in American crow blood films. Fish crow blood films contained Plasmodium relictum Celli and Sanfelice. Prior to this study, T. avium and P. relictum had not been reported from fish crows.

A comparison of the blood parasites in three subspecies of the yellow wagtail Motacilla flava.

One-hundred and eighty yellow wagtails Motacilla flava belonging to 3 subspecies (Motacilla flava feldegg, Motacilla flava flava, Motacilla flava thunbergi) were caught during the spring migration in south Kazakhstan and investigated by microscopic examination of stained blood smears. Haemoproteus anthi, Haemoproteus motacillae, Leucocytozoon fringillinarum, Leucocytozoon majoris, Plasmodium relictum, Plasmodium polare, Atoxoplasma sp., Trypanosoma sp., and microfilariae were identified. The overall prevalence of infection was 47.8%. Prevalences of Haemoproteus spp. (27.2%), Plasmodium spp. (25.0%), Leucocytozoon spp. (8.9%), Atoxoplasma spp. (4.4%), Trypanosoma spp. (1.1%), and microfilariae (0.6%) were recorded. No differences were discernible in parasite fauna or intensities of infection between males and females or between different subspecies. However, prevalence of infection of Haemoproteus, Leucocytozoon, and Plasmodium spp. was different in different host subspecies. These differences can be explained by differences in geographical location of breeding areas of these birds.

Pathogenicity, Serological Responses, and Diagnosis of Experimental and Natural Malarial Infections in Native Hawaiian Thrushes

AbstractOmao (Myadestes obscurus) from the Hawaiian Islands typically have very low prevalences of infection with avian malaria (Plasmodium relictum) and it is not clear whether they share the same high susceptibility to this parasite that has been documented in native Hawaiian honeycreepers. We exposed four captive Omao to single infective mosquito bites and measured parasitemia, serological responses, and mortality over time. All four birds experienced transient infections with low parasitemias and were immune when rechallenged with multiple infective mosquito bites. By contrast, three of four honeycreepers (Maui Alauahio, Paroreomyza montana) that were exposed to the same dose and parasite isolate succumbed to infection. All four Omao developed antibodies to a common suite of malarial antigens that were detectable on immunoblots of a crude red blood cell extract of P. relictum. We used this technique to screen plasma samples from wild Omao and endangered Puaiohi (Myadestes palmeri) that were captured at elevations between 900 and 1300 m on the islands of Hawaii and Kauai. We found that the true prevalence of infection at elevations where active malaria transmission occurs is much higher than estimates based on blood smears alone. Hawaiian thrushes appear to have a high tolerance for malaria, with most individuals developing chronic, low-level infections after exposure that cannot be diagnosed accurately by blood smears.

PATHOGENICITY, SEROLOGICAL RESPONSES, AND DIAGNOSIS OF EXPERIMENTAL AND NATURAL MALARIAL INFECTIONS IN NATIVE HAWAIIAN THRUSHES1

Omao (Myadestes obscurus) from the Hawaiian Islands typically have very low prevalences of infection with avian malaria (Plasmodium relictum) and it is not clear whether they share the same high susceptibility to this parasite that has been documented in native Hawaiian honeycreepers. We exposed four captive Omao to single infective mosquito bites and measured parasitemia, serological responses, and mortality over time. All four birds experienced transient infections with low parasitemias and were immune when rechallenged with multiple infective mosquito bites. By contrast, three of four honeycreepers (Maui Alauahio, Paroreomyza montana) that were exposed to the same dose and parasite isolate succumbed to infection. All four Omao developed antibodies to a common suite of malarial antigens that were detectable on immunoblots of a crude red blood cell extract of P. relictum. We used this technique to screen plasma samples from wild Omao and endangered Puaiohi (Myadestes palmeri) that were captured at elevations between 900 and 1300 m on the islands of Hawaii and Kauai. We found that the true prevalence of infection at elevations where active malaria transmission occurs is much higher than estimates based on blood smears alone. Hawaiian thrushes appear to have a high tolerance for malaria, with most individuals developing chronic, low-level infections after exposure that cannot be diagnosed accurately by blood smears.

Serological responses and immunity to superinfection with avian malaria in experimentally-infected Hawaii amakihi.

Six of seven Hawaii Amakihi (Hemignathus virens) with chronic malarial infections had no increases in peripheral parasitemia, declines in food consumption, or loss of body weight when rechallenged with the homologous isolate of Plasmodium relictum 61 to 62 days after initial infection. Five uninfected control amakihi exposed at the same time to infective mosquito bites developed acute infections with high parasitemias. Reductions in food consumption and loss of body weight occurred in all control birds and three of these individuals eventually died. When surviving birds were rechallenged >2 yr later with either the same parasite isolate or an isolate of P. relictum collected on the island of Kauai, all individuals were immune to superinfection. Chronically infected birds developed antibodies to a common suite of malarial antigens ranging in size from 22 to 170 kDa that were detectable as early as 8 days post infection on immunoblots of SDS-polyacrylamide gels. Antibodies to this suite of malarial antigens persisted as long as 1,248 days after initial infection and were consistently detectable at times when parasites were not easily found by microscopy on Giemsa-stained blood smears. The immunoblotting method that is described here appears to be an effective technique for identifying birds with chronic, low-intensity malarial infections when circulating parasites are not easily detectable by microscopy. Hawaiian honeycreepers that are capable of recovering from acute infections develop concomitant immunity to superinfection, making them functionally immune in areas where malaria transmission has become endemic.

Pathogenicity of avian malaria in experimentally-infected Hawaii Amakihi.

The introduction of avian malaria (Plasmodium relictum) and mosquitoes (Culex quinquefasciatus) to the Hawaiian Islands (USA) is believed to have played a major role in the decline and extinction of native Hawaiian honeycreepers (Drepanidinae). This introduced disease is thought to be one of the primary factors limiting recovery of honeycreepers at elevations below 1,200 m where native forest habitats are still relatively intact. One of the few remaining species of honeycreepers with a wide elevational distribution is the Hawaii Amakihi (Hernignathus virens). We measured morbidity and mortality in experimentally-infected Hawaii Amakihi that were captured in a high elevation, xeric habitat that is above the current range of the mosquito vector. Mortality among amakihi exposed to a single infective mosquito bite was 65% (13/20). All infected birds had significant declines in food consumption and a corresponding loss in body weight over the 60 day course of the experiment. Gross and microscopic lesions in birds that succumbed to malaria included enlargement and discoloration of the spleen and liver and parasitemias as high as 50% of circulating erythrocytes. Mortality in experimentally-infected amakihi was similar to that observed in Apapane (Himnatione sanguinea) and lower than that observed in Iiwi (Vestiaria coccinea) infected under similar conditions with the same parasite isolate. We conclude that the current elevational and geographic distribution of Hawaiian honeycreepers is determined by relative susceptibility to avian malaria.

New Data on the Morphology of Bird Haemoproteids Haemoproteus Bucerotis and H. Burhini (Haemosporida: Haemproteidae) with Remarks on the Status of H. Mcleani

New data on the morphology of bird haemoproteids (Sporozoa: Haemoproteidae) Haemoproteus bucerotis and H. burhini, which provide the opportunity to identify species of these parasites without the knowledge of the family to which their vertebrate hosts belong, are given. Illustrations of the main stages of development of gametocytes, available in the type material, are presented. The hapantotype of H. mcleani contains gametocytes and erythrocytic meronts of the malaria parasite belonging to the Plasmodium relictum group. Until additional material is available, H. mcleani is declared to be a species inquirenda.

Hematozoa in two populations of the threatened red-billed chough in Spain.

The prevalence of hematozoa in two populations of red-billed choughs (Pyrrhocorax pyrrhocorax) was sampled in 1992 and 1994 in Spain. Two blood parasites infected red-billed choughs. A species of Plasmodium, possibly Plasmodium relictum, and the piroplasm Babesia frugilegica, are described for the first time from this host. Low prevalence (1/178, < 1%) of hematozoa in these populations, was evidence for a lack of effects of blood parasites on the life history and conservation of this threatened species in at least the two populations studied.

Parasite diversity in an endemic region for avian malaria and identification of a parasite causing penguin mortality.

Understanding the population structure of Plasmodium parasites is essential for malaria intervention. A survey of parasites in vectors and host infections was conducted in an area of intense mortality due to malaria in a captive penguin (Spheniscus demersus) colony, using a novel method for identification of Plasmodium species by amplification of ribosomal sequences in DNA or RNA. Three phylogenetically distinct groups of avian Plasmodium were detected in mosquitoes (Culex) collected at the study site (Baltimore Zoo, Baltimore, MD) during a period of high transmission. One of the three clades of Plasmodium was found to be prevalent in penguins monitored through the malaria transmission season and consistent with morphological identification as Plasmodium relictum. This parasite sequence was directly associated with the death of a penguin. Thus, a complete transmission cycle is defined at this site. Phylogenetic comparison of ribosomal sequences to an authenticated reference strain of Plasmodium relictum indicates that this is not the parasite causing death in the penguins, suggesting that different parasites may be morphologically indistinguishable.

A model for the prediction of relative titres of avian malaria and Aspergillus spp. IgG in Jackass penguin ( Spheniscus demersus) females based on maternal IgG in egg-yolk

A model for the prediction of IgG titres in females of the Jackass penguin ( Spheniscus demersus) was developed, based on IgG which was maternally tranemitted to the yolk of urembryonated eggs produced by these females. However, prediction of the female titre based on the titre of embryonated eggs may be inadequate. Blood samples from 10 S. demersus females and their corresponding embryonated ( n=10) and unembryonated ( n=49) eggs were analysed by indirect ELISA for avian malaria ( Plasmodium relictum, P. elongatum) IgG and Aspergillus spp. IgG. There was no correlation between humoral responses to avian malaria and Aspergillus spp. in females or in their eggs. Avian malaria and Aspergillus spp. titres were significantly higher ( P<0.05) in the eggs than in the corresponding females and were significantly correlated ( P<0.01) with the blood titres, r=0.84, r=0.89, respectively. No correlation was found between titres of embryo yolk-sac (embryonated eggs) and the blood of their female parent; however, the embryo blood and the corresponding female titres were significantly ( P<0.05) correlated (avian malaria, r=0.74; Aspergillus spp., r=0.69). Blood and the corresponding egg-yolk (unembryonated eggs) IgG titres regressed significantly ( P<0.01). Female IgG titre ( y) is related to (unembryonated) egg-yolk IgG titre by the significant ( P<0.05) regression y=−0.61+1.46 X for avian malaria, and y=−0.02+0.85 X for Aspergillus spp., with ±95% prediction limits of ±0.15 and ±0.12, respectively. This model provides access to serological information on the remote free-ranging Jackass penguins and captive Jackass-peaguin colonies without the necessity of stressful blood collection.

Characteristics of Naturally Acquired Plasmodium relictum capistranoae Infections in Naive Hawaiian Crows (Corvus hawaiiensis) in Hawaii

Indigenous to Hawaii, the Hawaiian crow (Corvus hawaiiensis) is the world's most severely endangered species with only 3 reproductively active pairs remaining in the wild. Seven captive-reared, avian malaria-naive C. hawaiiensis were exposed in an outdoor aviary and hematologically and serologically monitored for 9 wk. Three birds showed Plasmodium relictum capistranoae parasitemia (6.35%, 2.15%, and 0.60%). All birds were seroconverted for malaria on week 7 as determined by enzyme-linked immunosorbent assay (ELISA). Malaria IgG levels of exposed parasitemic birds did not differ from those of exposed nonparasitemic C. hawaiiensis and were not significantly correlated with the level of parasitemia. Four of 9 hematological parameters, e.g., white blood cell count (WBC), relative and absolute lymphocytosis, and total solids (TS), showed significant increases related to ELISA-determined malarial infection. The sensitivity, specificity, and the positive predictive values of these 4 parameters for malarial infections in C. hawaiiensis were higher than 66%, with the WBC and TS sensitivity reaching 100%. The reference range of 9 hematological parameters was established based on uninfected, clinically healthy C. hawaiiensis. Seven birds were successfully treated and released, increasing the total wild C. hawaiiensis world population by approximately 50%.

Evaluation of serum chemistry values associated with avian malaria infections in African black-footed penguins (Spheniscus demersus)

The value profiles of 5 intracellular enzymes, 15 metabolites (with 2 associated ratios), and 3 electrolytes were monitored over time in 9 captive-reared African black-footed penguins (Spheniscus demersus) with different avian malaria clinical status: uninfected, subclinically infected, and clinically infected with fatal outcome. Fatal infections were caused by Plasmodium relictum. Numerous schizonts were visible in the lungs, liver, spleen, and interstitial tissue of the kidneys. The reference ranges of 23 serum clinical chemistry parameters and 2 ratios were established for S. demersus. The mean values obtained for 8 of 23 parameters of the infected penguins were significantly different from those recorded for the uninfected birds, indicating impaired renal function, hepatic dysfunction, and nonspecific tissue damage related to the infestation with exoerythrocytic schizonts. Analysis of sensitivity, specificity, and negative and positive predictive values (PPVs) showed that gamma-glutamyltranspeptidase (GGTP), alanine aminotransferase (ALT), and creatinine reached PPVs and a specificity over 57% for avian malaria infections in penguins. Creatinine, ALT, and GGTP values should be consulted in evaluation of the clinical malaria status of S. demersus.