Populations of Leucocytozoon Gametocytes in Blue Grouse (Dendragapus obscurus) from Hardwicke Island,British Columbia1

Population dynamics of round and elongate gametocytes of Leucocytozoon in wild and captive blue grouse (Dendragapus obscurus (Say)) from Hardwicke Island, British Columbia, were studied from 1980 to 1982. Blue grouse chicks were sampled weekly throughout each transmission season. Three patterns in the type of gametocyte produced during primary infection were observed in naturally-infected captive and wild blue grouse chicks. Such variation in the expression of the gametocyte stage within a single host population suggests a different interpretation than has been previously reported for species of Leucocytozoon. The data from the primary patterns and profiles coupled with reexposure data and the asynchronous appearance of round and elongate gametocytes can be best interpreted as infection with two concurrent species of Leucocytozoon in blue grouse. More detailed research on the life cycle is necessary to confirm if two species of Leucocytozoon exist in blue grouse.     

Gametocytogenesis of Leucocytozoon Smithi

ABSTRACT. Development of young gamelocytes of Leucocytozoon smithi into morphologically mature forms was studied using electron microscopy. Gametocytogenesis began on day seven post inoculation when merozoites, released from ruptured hepatic schizonts, developed into gametocytes within mononuclear phagocytes or leukocytes (monocytes or lymphocytes). No gametocytes were observed in any erythrocytes or polymorphonuclear leukocytes. Two gametocyte forms, round and elongate, were observed. Immature round gametocytes occurred on days 7-10 post inoculation in the deep vasculature of liver, lung and spleen. Mature elongate gametocytes were observed beginning on day 12 post inoculation in both the deep tissue vasculature and peripheral circulation of the turkey host. Growth and elongation of the gametocyte resulted in distortion of the host cell and its nucleus. the host cell nucleus initially was elongated and displaced to one side or indented by the growing parasite. Eventually, the nucleus was laterally compressed or split into two or three fragments. the compressed host cell cytoplasm was displaced longitudinally and stretched over the parasite to form hornlike cytoplasmic extensions from each end. the potential role of microtubules in the elongation of the gametocyte and its host cell, and possibly in the indentation and splitting of the host cell nucleus, is discussed.     

Leucocytozoonosis in Canada geese in upper Michigan,. 1. Strain differences among geese from different localities.

Geographic variation in pathogenicity of Leucocytozoon simondi in Canada geese (Branta canadensis maxima) was investigated by exposing goslings to natural infection at three locations in the upper peninsula of Michigan. Examination of blood smears and tissue sections revealed two patterns of development. Hepatic schizogony and secondary megaloschizogony occurred in cells of the reticuloendothelial system, with round and elongate gametocytes, or only hepatic schizonts and round gametocytes. The evidence for strain differences in L. simondi and its implications in wildfowl management practices are discussed.     

Elongate and Round Gametocytes of Leucocytozoon simondi (Mathis & Léger) in Ducks Inoculated with Megaloschizonts

SYNOPSIS. Single megaloschizonts give rise to elongate and round gametocytes, the former outnumbering the latter. Male and female elongate gametocytes develop from merozoites of a single megaloschizont. Elongate gametocytes were seen 2–7 days and round gametocytes 6–11 days after megaloschizonts had been inoculated into ducklings. Experimental evidence indicates that merozoites of megaloschizonts invade blood cells and develop into elongate gametocytes. Other merozoites infect tissue cells and develop into secondary exoerythrocytic schizonts which give rise to round gametocytes. Relapse in Leucocytozoon simondi infections is discussed in relation to megaloschizont-induced exoerythrocytic schizogony.     

Anemia in Ducks Infected with Leucocytozoon simondi*†

SYNOPSIS. Thirty-four white Pekin ducklings were used to study the anemia associated with infection by Leucocytozoon simondi. The first appearance of gametocytes in the peripheral blood, as detected by thin smears, marked the onset of anemia. This anemia lasted for the duration of the initial parasitemia, usually reaching a low point early in the infection (1 to 5 days post patency) and returning slowly to normal as the parasitemia decreased. Greatest gametocyte density occurred 5 to 8 days post patency. In a number of cases recovery from anemia began simultaneously or even prior to the highest level in the gametocyte density. In low level parasitemias a fluctuation occurred in erythrocyte numbers which corresponded with the peaks of gametocyte density. In none of the infections was a sufficient number of parasite observed to account for the existing anemia. Haemopoietic activity was observed for a brief period at the time of maximum erythrocyte loss in only a few birds. The overcompensation for erythrocyte loss at the end of the primary parasitermia favors the view that increased erythrocyte production may account for the short duration of haemopoiesis.     

Schizogony and Gametogony of Leucocytozoon simondi and Associated Reactions in the Avian Host*

SYNOPSIS. Stages of development of Leucocytozoon simondi in White Pekin ducklings and their reactions to the parasite were studied on successive days after infecting them artificially with sporozoites from Simulium rugglesi. The minimum prepatent period was 5 days. The first asexual cycle occurred exclusively in the parenchymal cells of the liver. Progeny of these hepatic schizonts followed one of 3 courses: (a) invaded parenchymal liver cells to give rise to another hepatic cycle, (b) penetrated blood cells to form round gametocytes, and (c) were phagocytized by macrophages and grew into megaloschizonts thruout the body. The appearance of elongating gametocytes coincided with the period of maturation and release of merozoites from the megaloschizonts. Experimental evidence supports the hypothesis that the round gametocytes arise from the hepatic schizonts and the elongate forms from the megaloschizonts. Mature megaloschizonts released millions of merozoites, but a high 2nd peak in parasitemia did not develop because of retention of developing gametocytes in the deep circulation, particularly the liver and spleen, and a pronounced host reaction.     

Hematozoa of waterfowl from Michigan

Two hundred eighteen and 127 wild waterfowl (Anatidae) of five species were sampled from the Kellogg Biological Station area (Michigan, USA) during the summer (1 June to 24 August 1995) and fall (9 September to 8 October 1995), respectively. Twelve (6%) of those sampled in summer and 13 (11%) sampled in the fall were infected with hemosporids. Haemoproteus nettionis, Haemoproteus greineri, and Leucocytozoon simondi infected both summer and fall birds, with H. nettionis the most common (4% summer; 7% fall). Mean intensities were low; the highest mean intensity was 4.6+/-1.1 gametocytes per 5,000 uninfected erythrocytes for H. nettionis in summer. Of 123 local waterfowl, none were infected with any blood parasite. Thirty-five captive year-round resident waterfowl also were sampled and no blood parasites were found.     

Blood parasites of blue grouse (Dendragapus Obscurus) in western North America

Three hundred thirty-three blue grouse (Dendragapus obscurus) were examined for blood parasites from 11 sites: southern Yukon Territory, southeast coastal Alaska, northern and central interior British Columbia, south coastal British Columbia, northcentral Washington, southcentral Oregon, northwestern California, eastcentral Nevada, northwestern Colorado, and westcentral Montana. Three species of protozoan parasites (Leucocytozoon lovati, Haemoproteus mansoni, Trypanosoma avium) and a splendidofilariid nematode (Microfilaria sp. B) were found in nearly all locations. Prevalence levels were consistently high for L. lovati (92%). The other hematozoa were found less frequently (H. mansoni 29%; T. avium 46%; and microfilaria 29%). The range of these parasites in blue grouse was extended to a more northern (Yukon Territory) and more southern distribution (Nevada than previously reported. Ranges were also extended to blue grouse populations in Alaska, Washington, Oregon and California.     

A SURVEY OF BLOOD PARASITES OF BIRDS IN THE MASCARENE ISLANDS, INDIAN OCEAN: WITH DESCRIPTIONS OF TWO NEW SPECIES AND TAXONOMIC DISCUSSION

A survey was carried out on the prevalence of blood parasites in birds in the Mascarene Islands. Smears from 357 birds of 25 species in 12 families were examined, of which 150 (42%) were found to harbour blood parasites. The most common parasites were Leucocytozoon ; a new species, L. zosteropis , is described from the Grey White-eye Zosterops borbonica mauritiana. This parasite was observed in smears from 68 birds of three species: Z. borbonica, Z. chloronothos and Z. olivacea. Other species of Leucocytozoon identified were L. fringillinarum from fodies, sparrows and a bulbul and L. marchouxi from two doves.
Haemoproteus was found only in domestic pigeons Columba livia and identified as H. columbae. Plasmodium relictum, P. vaughani and an unidentified species with elongate gametocytes were found in Zosterops , and Plasmodium sp. of low infection observed in other hosts. Trypanosoma mayae is redescribed from the House Sparrow Passer domesticus and the Mauritius Fody Foudia rubra , and considered to be a valid species. A new species of trypanosome, Trypanosoma phedinae , is described from the Malagasy Swallow Phedina b. borbonica. Other birds were found to harbour low infections of unidentified species of trypanosomes. A small number of birds were infected with Atoxoplasma , haemogregarines and Rickettsia-like organisms. An unidentified organism with a predilection for eosinophils was observed in several Mascarene Swiftlets Collocalia francica.
The results are discussed in relation to the possible effects of the parasites on the birds of the Mascarene Islands and comparisons made with the results of similar surveys on other Indian Ocean Islands.     

Changes in Haemoproteus sex ratios: fertility insurance or differential sex lifespan?

There is little direct evidence of the fitness effects of changes in malaria gametocyte sex ratio. Gametocyte sex ratios in haemospororin parasites (phylum Apicomplexa) are usually female skewed. However, in some cases and especially in Haemoproteus parasites, less female-biased and even male-biased sex ratios are encountered. The 'fertility insurance hypothesis' tries to explain these biases as an evolutionary strategy to facilitate gamete encounter. Thus, the hypothesis predicts that, if there is a reduction in gametocyte density (intensity of infection) or other factors preventing gametes from meeting, a change to a higher proportion of male gametocytes may be favoured. By contrast, a change in sex ratio may be caused by other non-adaptive mechanisms, for example differential survival of the gametocytes of each sex. We study within-host changes in Haemoproteus majoris sex ratios following an experimental reduction in the density of the parasites in the blood in a breeding population of blue tits (Parus caeruleus). Medication with the antimalarial drug primaquine induced a significant reduction in Haemoproteus gametocyte infection intensity in two different breeding seasons and under two different doses of medication. Sex ratios became male skewed following the experimental treatment in agreement with the predictions of the 'fertility insurance' hypothesis. Also in support of the hypothesis, a significant change towards male-biased sex ratios emerged for non-medicated birds in one year, probably owing to the natural immune reduction of the density of the parasites in the blood. The alternative possibility that changes are caused by different lifespans of gametocytes is not supported by changes in sex ratios in control hosts, where new production and release of gametocytes occur.     

Plasmodium chabaudi: effect of antimalarial drugs on gametocytogenesis.

The proportion of asexual blood-stage malaria parasites that develop into transmission stages (gametocytes) can increase in response to stress. We investigated whether stress imposed by a variety of antimalarial drugs administered before or during infection increased gametocyte production (gametocytogenesis) in vivo in the rodent malaria parasite, Plasmodium chabaudi. All methods of drug treatment greatly reduced the numbers of asexual parasites produced during an infection but resulted in either no reduction in numbers of gametocytes or a smaller reduction than that experienced by asexuals. We used a simple model to estimate temporal variation in gametocyte production. Temporal patterns of gametocytogenesis did not greatly differ between untreated and prophylaxis infections, with rates of gametocytogenesis always increasing as the infection progressed. In contrast, administration of drugs 5 days after infection stimulated increased rates of gametocytogenesis early in the infection, resulting in earlier peak gametocyte densities relative to untreated infections. Given the correlation between gametocyte densities and infectivity to mosquito vectors, and the high frequency of subcurative drug therapy and prophylaxis in human populations, these data suggest that antimalarial drugs may frequently have only a small effect on reducing malaria transmission and may help to explain the rapid spread of drug-resistant geno-types.     

A Haemocystidium species from the East African gecko Lygodactylus capensis grotei

Haemocystidium lygodactyli n. sp. parasitizes Lygodactylus capensis grotei (Gekkonidae) in Tanzania. Mature gametocytes in acute phase of infection average 16.3 x 5.7 microm (11-20 x 4-9.5 microm), with LW 93.0 (62-140 microm2) and L/W ratio 2.94 (1.2-3.9). Gametocytes usually lateral, lateropolar, or halteridial in position. There was no significant sexual dimorphism in gametocyte dimensions. Nuclei discrete in both sexes at maturity, with a rounded nucleolus usually present in microgametocytes. In chronic infection, gametocytes were 18.1 x 8.7 microm (8-25 x 5-11 microm), with LW 156.8 microm2 (80-250) and L/W 2.16 (1.1-3.6). When gametocytes from the chronic infection were compared with the same sex in acute infection, length did not differ, but differences were present between the same sex in each comparison of width, LW, and L/W. Macrogametocytes and microgametocytes in chronic phase were broader, larger, and less elongate and most commonly halteridial. Meronts were found only in endothelium and connective tissue of lung. Elongate to oval in shape, the larger meronts filled with nuclei were 12.2 x 6.9 microm (10.0 x 5.0-16.0 x 9.0), with LW 50-144 microm2 (85.1). In 1 initial infection followed for 49 days, apparently mature gametocytes appeared by day 28 postcapture. Binucleate parasites were present from day 14 throughout the course of infection, with their frequency increasing from 5% of immature parasites to 34% of mature gametocytes. Binucleate mature gametocytes were found in 1 other infection, where 14% had 2 nuclei. Sex ratio varied from 51 to 63% in favor of macrogametocytes.     

Leucocytozoon in the Avian Order Columbiformes, with a Description of L. marchouxi Mathis and Leǵer 1910 from the Mourning Dove

Leucocytozoon marchouxi is described from the mourning dove, Zenaidura macroura carolinensis in Illinois. The macrogametocytes are rounded or elliptical, measuring 7 to 11 by 8 to 15 microns (mean, 9 by 12 microns), and stain dark blue with Giemsa stain. The microgametocytes are often distorted or ruptured by the smearing process, but if not badly injured measure 5 to 11 by 8 to 15 microns, (mean, 8 by 11 microns). They stain pale blue with Giemsa stain. Host cell cytoplasm is rarely seen surrounding the microgametocytes, but was found in 26% of cells parasitized by the macrogametocytes. When present it forms a narrow border around part or all of the parasite's periphery, and is not drawn out to form elongate "horns."
The parasite was found in ten birds, of which five were adults, one was a juvenile, and four were nestlings. The infections were relatively light in the adults. The youngest bird in which the protozoon was found was 14 days old.
The literature on Leucocytozoon in the avian order Columbiformes is reviewed. All forms with rounded gametocytes so far reported are considered to be L. marchouxi Mathis and Leger, 1910, of which L. turtur Covaleda Ortega and Gallego Berenguer, 1946, is considered a synonym.     

Male gametocyte fecundity and sex ratio of a malaria parasite, Plasmodium mexicanum

Evolutionary theory predicts that the sex ratio of Plasmodium gametocytes will be determined by the number of gametes produced per male gametocyte (male fecundity), parasite clonal diversity and any factor that reduces male gametes' ability to find and combine with female gametes. Despite the importance of male gametocyte fecundity for sex ratio theory as applied to malaria parasites, few data are available on gamete production by male gametocytes. In this study, exflagellating gametes, a measure of male fecundity, were counted for 866 gametocytes from 26 natural infections of the lizard malaria parasite, Plasmodium mexicanum. The maximum male fecundity observed was 8, but most gametocytes produced 2-3 gametes, a value consistent with the typical sex ratio observed for P. mexicanum. Male gametocytes in infections with higher gametocytaemia had lower fecundity. Male fecundity was not correlated with gametocyte size, but differed among infections, suggesting genetic variation for fecundity. Fecundity and sex ratio were correlated (more female gametocytes with higher fecundity) as predicted by theory. Results agree with evolutionary theory, but also suggest a possible tradeoff between production time and fecundity, which could explain the low fecundity of this species, the variation among infections, and the correlation with gametocytaemia.     

The saurian malarias of Venezuela: Haemosporidian parasites of gekkonid lizards

Telford S. P., Jr. 1978. The saurian malarias of Venezuela: haemosporidian parasites of gekkonid lizards. International Journal for Parasitology8: 341–353. Five haemosporidian species were found among 185 gekkonid lizards from Estados Portuguesa, Cojedes and Aragua, Venezuela, four of which were new to science. A pigmented Plasmodium species is described from Gonatodes taniae of Estado Aragua. It produces 8–20 merozoites in variably shaped schizonts, and elongate, irregularly margined prematuration gametocytes which contract to form round to broadly elongate mature gametocytes. Phyllodactylus ventralis of Estado Portuguesa is parasitized by two new unpigmented malarial species. One produces 11–35 merozoites in schizonts which are often rounded or elongated, occasionally fan-shaped. Gametocytes are always elongated and usually lie diagonally across one end of the host cell or laterally to the nucleus. The second species forms rounded mature schizonts nearly filled with 14–32 merozoites. The sexual stages are usually round or oval, rarely elongate. Plasmodium aurulentum Telford, 1971 was found in Thecadactylus raplcaudus of Estados Portuguesa and Cojedes. A single Thecadactylus from Cojedes was infected by a haemosporidian species of uncertain generic identity which resembles a parasite found earlier in a Panamanian gecko.     

The fine structure of elongate gametocytes of Leucocytozoon ziemanni (Laveran).

In an effort to establish comparative data within the genus Leucocytozoon, elongate gametocytes of L. ziemanni from naturally infected great horned owls (Bubo virginianus) were examined by electron microscopy. Micro- and macrogametocytes proved to be easily distinguishable at the electron microscopic level due to dramatic dimorphism at maturity and cytoplasmic and nuclear morphology. The parasite membrane architecture, number and type of cytoplasmic ribosomes of both micro- and macrogametocytes, presence and arrangement of osmiophilic bodies and electron dense spheres, mitochondrial morphology, endoplasmic reticulum cisternae morphology, mitochondria containing pocket infoldings of the nuclear membrane of the microgametocytes, and cytostome and food vacuole formation compare favorably with available information on L. simondi and L. smithi. Comparative variations exist only in that L. ziemanni gametocytes apparently lack compartmentalization of the cytoplasm by aligned unit membranes and parasite induced separations of the host cell nucleus as reported for L. simondi.     

Development of restoration techniques for Hawaiian thrushes: Collection of wild eggs,artificial incubation,hand‐rearing,captive‐breeding,and re‐introduction to the wild

From 1995 to 1999, two species of endemic Hawaiian thrushes, `Oma`o (Myadestes obscurus) and Puaiohi (M. palmeri), were captive‐reared and re‐introduced into their historic range in Hawai`i by The Peregrine Fund, in collaboration with the U.S. Geological Survey–Biological Resources Division (BRD) and the Hawai`i State Department of Land and Natural Resources. This paper describes the management techniques that were developed (collection of wild eggs, artificial incubation, hand‐rearing, captive propagation, and release) with the non‐endangered surrogate species, the `Oma`o; techniques that are now being used for recovery of the endangered Puaiohi. In 1995 and 1996, 29 viable `Oma`o eggs were collected from the wild. Of 27 chicks hatched, 25 were hand‐reared and released into Pu`u Wa`awa`a Wildlife Reserve. Using the techniques developed for the `Oma`o, a captive propagation and release program was initiated in 1996 to aid the recovery of the endangered Puaiohi. Fifteen viable Puaiohi eggs were collected from the wild (1996–1997) to establish a captive breeding flock to produce birds for re‐introduction. These Puaiohi reproduced for the first time in captivity in 1998 (total Puaiohi chicks reared in captivity 1996–1998 = 41). In 1999, 14 captive‐bred Puaiohi were re‐introduced into the Alaka`i Swamp, Kaua`i. These captive‐bred birds reproduced and fledged seven chicks in the wild after release. This is the first endangered passerine recovery program using this broad spectrum of management techniques (collection of wild eggs, artificial incubation, hand‐rearing, captive‐breeding, and release) in which re‐introduced birds survived and bred in the wild. Long‐term population monitoring will be published separately [BRD, in preparation]. Zoo Biol 19:263–277, 2000. © 2000 Wiley‐Liss, Inc.     

Ultrastructural Study of Gametocytes and Gametogenesis of Haemoproteus metchnikovi

SYNOPSIS. The ultrastructure of gametocytes and microgametogenesis of Haemoproteus metchnikovi , an intracellular malaria parasite of chelonians, was compared with other malarial parasites. Gametocytes resemble those described for other avian, reptilian and mammalian malarial parasites. The process of microgametogenesis is similar in many respects to that reported for Leucocytozoon simondi (Aikawa et al., 1970) and Haemoproteus columbae (Bradbury and Trager, 1968). Atypical centrioles are described from both microgametocytes and macrogametocytes. Axoneme development begins before the microgametocyte leaves the host red blood cell. Fully developed microgametes which bud off from the parent gametocyte contain a single axoneme with the typical 9 + 2 pattern of microtubules.     

Leucocytozoon lovati infections in wild rock ptarmigan (Lagopus mutus) in Japan

Leucocytozoon lovati infections were detected in free-flying rock ptarmigan (Lagopus mutus), an endangered species that inhabits alpine areas in Japan. Eight of nine adult birds tested positive for L. lovati infection. For comparison, two captive rock ptarmigans hatched in a breeding facility at the foot of the mountains were examined. Both were negative for L. lovati infection. This is the first report of L. lovati infection in the rock ptarmigan in Japan.     

Plasmodium (Huffia) hermani sp. n. from wild turkeys (Meleagris gallopavo) in Florida*

SYNOPSIS. Plasmodium (Huffia) hermani sp. n. is described from wild turkeys (Meleagris gallopavo Linnaeus) in Florida. It produces rounded schizonts with 6–14 nuclei arranged peripherally as a rosette and elongate, slender gametocytes with irregular margins. Asexual stages parasitize all cells in the erythrocyte series and, in heavy infections, predominantly occur in erythroblasts and their precursors. Presence and degree of pigmentation vary with maturity of the host cell. Gametocytes occupy erythrocytes only, with pigment dispersed in black granules throughout the cytoplasm. Cells containing schizonts are often rounded and enlarged and those parasitized by gametocytes may be somewhat distorted in shape by lateral hypertrophy. Host cell nuclei may be displaced, but are not distorted, except slightly by pressure from the parasite. Plasmodium hermani differs from P. (Giovannolaia) durae by producing low level (> 6%), nonlethal parasitemias in turkey poults, an absence of phanerozoites in capillary endothelium of the brain and viscera, and inability to infect chicks. Plasmodium hermani is more like P. (Huffia) elongatum in gametocyte morphology, schizogony in all types of erythrocyte precursors, with gametocytes occurring in erythrocytes only, and concentration of schizonts in heavy infections in bone marrow and spleen. It differs from P. elongatum by its lack of infectivity to passeriform and anseriform hosts and by a strong immune response which develops in infected birds.