Populations of Leucocytozoon gametocytes in blue grouse (Dendragapus obscurus) from Hardwicke Island, British Columbia

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.     

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.     

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.     

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.     

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.     

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.     

Plasmodium spp. (Apicomplexa: Plasmodiidae) of the flying lizardDraco volans (Agamidae)

The agamid lizardDraco volans from Palawan, Republic of the Philippines, was found to be parasitised by threePlasmodium species:P. draconis n. sp.,P. volans n. sp. andP. vastator, Laird 1960. BothP. draconis andP. volans, but notP. vastator, were also present inD. volans from Sarawak. The species are readily distinguished by schizont size, merozoite number, and gametocyte size and shape.P. volans has schizonts approximately one-half the size of those ofP. draconis and produces 4–6 merozoites in comparison to 4–16 in the larger species. Gametocytes of both new species are predominantly oval in the Palawan sample and elongate in that from Sarawak.P. draconis gametocytes are approximately twice the size ofP. volans gametocytes, but on average no more than one-half the size of gametocytes ofP. vastator.     

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.     

A comparison of pedigree‐ and DNA‐based measures for identifying inbreeding depression in the critically endangered Attwater's Prairie‐chicken

The primary goal of captive breeding programmes for endangered species is to prevent extinction, a component of which includes the preservation of genetic diversity and avoidance of inbreeding. This is typically accomplished by minimizing mean kinship in the population, thereby maintaining equal representation of the genetic founders used to initiate the captive population. If errors in the pedigree do exist, such an approach becomes less effective for minimizing inbreeding depression. In this study, both pedigree‐ and DNA‐based methods were used to assess whether inbreeding depression existed in the captive population of the critically endangered Attwater's Prairie‐chicken (Tympanuchus cupido attwateri), a subspecies of prairie grouse that has experienced a significant decline in abundance and concurrent reduction in neutral genetic diversity. When examining the captive population for signs of inbreeding, variation in pedigree‐based inbreeding coefficients (f_pedigree) was less than that obtained from DNA‐based methods (f_DNA). Mortality of chicks and adults in captivity were also positively correlated with parental relatedness (r_DNA) and f_DNA, respectively, while no correlation was observed with pedigree‐based measures when controlling for additional variables such as age, breeding facility, gender and captive/release status. Further, individual homozygosity by loci (HL) and parental r_DNA values were positively correlated with adult mortality in captivity and the occurrence of a lethal congenital defect in chicks, respectively, suggesting that inbreeding may be a contributing factor increasing the frequency of this condition among Attwater's Prairie‐chickens. This study highlights the importance of using DNA‐based methods to better inform management decisions when pedigrees are incomplete or errors may exist due to uncertainty in pairings.     

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.     

Blood parasites of blue grouse: variation in prevalence and patterns of interspecific association

Blood parasites of blue grouse (Dendragapus obscurus) were sampled and the factors responsible for variation in prevalence of blood parasites, and patterns of association among parasite species, were investigated. Five genera of haematozoa were surveyed including four protozoans (Haemoproteus, Leucocytozoon, Plasmodium, and Trypanosoma) and a nematode (Splendidofilaria). Prevalence of blood parasites varied significantly between years; sexes differed in number of parasite species in one of two years. Both positive and negative overall associations among all parasites were found when variance-ratio tests were used indicating that blood parasites often were not independent of one another. In general, Leucocytozoon and Trypanosoma often co-occurred; the strongest associations between these two parasites appeared in samples of hosts most heavily infected by other parasites. Negative associations between parasite species always involved Haemoproteus. Associations between pairs of species did not account wholly for overall patterns of associations within the parasite assemblage. Studies of associations within blood parasite assemblages are important for understanding the ecology of haemotropic infections and for clucidating the need for multi-parasite models of parasite-host interactions.     

Plasmodium octamerium n. sp., an Avian Malaria Parasite from the Pintail Whydah Bird Vidua macroura*

SYNOPSIS. A new species of avian malaria parasite is described from the pintail whydah Vidua macroura, a very small African finch of the weaver bird family (Ploceidae). Its structure has been studied chiefly in the canary, to which it is easily transmissible by blood inoculation. Since the segmenters most often produce 8 merozoites, the name Plasmodium octamerium n. sp. is proposed. Other characteristics include sexual stages which are usually elongate, often slender, and do not displace the host cell nucleus, and gametocytes indistinguishable from those of many species of Haemoproteus. Erythrocytes are the only blood cells parasitized. The new species resembles Plasmodium fallax in many respects, but gives rise to fewer merozoites and the asexual forms are smaller. Blood-induced infections are also of strikingly different type in some host species. Among susceptible host species are several kinds of finches, pigeons, quail, young chicks, chukars, tree and song sparrows. In most of these hosts infections are mild, but some tree sparrows die as the result of blood infection, and chukars usually die because of massive invasion of the capillary endothelium of the brain by exoerythrocytic forms. These are of the gallinaceum type and may be quite large, producing hundreds of merozoites. Exoerythrocytic stages were sought but not found in other host species.     

A Comparative Study of Gametocyte Ultrastructure in Avian Haemosporidia*

The fine structure of gametocytes of 3 avian haemosporidian parasites Plasmodium gallinaceum, Haemoproteus columbae, and Leucocytozoon simondi has been studied and compared by electron microscopy. The gametocytes of all 3 species are bounded by a 3-layered limiting membrane system, possess a cytostome during some portion of their residence within host cells, and their sex can be distinguished by both nuclear and cytoplasmic characteristics. L. simondi differs most significantly from P. gallinaceum and H. columbae in possessing large intranuclear granules, mitochondria associated with pocket infoldings of the nuclear envelope near the atypical centriole complex and compartmentalization of the cytoplasm by segments of closely aligned unit membranes. Further, the cytostome of L. simondi does not appear to be a persistent structure as in the other 2 species and pigment is not present within food vacuoles. L. simondi also is capable of infecting a wider variety of host cells and within leukocytes produces striations of the host nucleus and an apparent spiral banding of the host cell surface. The comparison of P. gallinaceum, H. columbae, and L. simondi gametocytes by electron microscopy leads to the conclusion that Plasmodium and Haemoproteus are more closely related to each other than either of them is on Leucocytozoon. The terminology used to describe certain organelles within the gametocyte's cytoplasm has been reexamined and the relationship of the nucleolus to parasite maturation also is described.     

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.     

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.     

Notes on New Zealand mammals 9: Long‐tailed bat (Chalinolobus tuberculatus) chased by morepork (Ninox novaeseelandiae)

Blood smears from 43 species of bird, mainly from the South Island of New Zealand, were examined for haematozoon parasites. An undescribed species of Leucocytozoon was discovered in the Fiordland crested penguin, Eudyptes pachyrhynchus. It is assigned the name Leucocytozoon tawaki, and the gametocytes are described. Preliminary observations of its development in Austrosimulium austra‐lense, A. dumbletoni, and A. ungulatum are discussed, and the ookinete, oocyst, and sporozoite stages within these hosts are briefly described.     

Iodine deficiency affects hatchability of endangered captive kaki (Black Stilt,Himantopus novaezelandiae)

A significant increase in hatching and late‐incubation deaths during two breeding seasons in a captive population of endangered black stilts (kaki, Himantopus novaezelandiae) prompted an investigation into the potential role of iodine deficiency. During the 1997 and 1998 breeding seasons, the survival rate of captive‐laid eggs during artificial incubation and hatching was lower than that of eggs laid by wild kaki, which were collected and incubated artificially in the same environment. Necropsy results revealed abnormalities in thyroid structure. These abnormalities had been occurring in captive birds since 1994, but they peaked in 1997 and 1998 at 30% and 81%, respectively, of all diagnosed necropsies. Necropsies of pied stilts, hybrids, and one kaki from the wild revealed no thyroid abnormalities. Gross morphological symptoms observed at hatching in chicks that died were consistent with those described for iodine deficiency in poultry. Serum levels of thyroxine (T4) were considerably higher in wild pied stilts and hybrid chicks than in captive adult, subadult, and kaki chicks. In five individuals from the captive population, serum levels increased after about 160 days of iodine supplementation and approached values in the wild. The constraints associated with working with such a critically endangered species (e.g., small sample size and an urgent need to effect changes) precluded the use of an experimental approach to determine the role iodine deficiency played in peri‐hatching deaths. However, we believe the evidence presented here strongly supports a case for the impact of iodine on survival within the captive population. Our experience also highlights the need for vigilance in captive programs with respect to potential dietary deficiencies when endangered species are raised in captivity for conservation purposes. Zoo Biol 23:1–13, 2004. © 2004 Wiley‐Liss, Inc.     

Captive breeding for reintroduction: influence of management practices and biological factors on survival of captive kaki (black stilt)

An important component of the restoration strategy for the critically endangered kaki or black stilt (Himantopus novaezelandiae) is captive breeding for release. Since 1981 1,879 eggs were collected from wild and captive pairs, with birds laying up to four clutches. Eggs were incubated artificially and most chicks reared by hand until released as juveniles (about 60 days) or sub‐adults (9–10 months). Because survival in captivity is a significant determinant of the number of birds available for release, we wished to identify sources of variation in mortality to assess potential impacts of management on productivity. Hatchability was 78% for captive‐laid eggs and 91% for wild‐laid eggs. Survival of hatched eggs was 82% by 10 months of age for both wild and captive birds. Most egg mortality occurred early in incubation and around hatching: the timing of mortality was unaffected by whether birds were captive or wild, hybrid or pure kaki, or when eggs were laid. Heavier hatchlings showed higher initial survival, as did chicks from wild parents. Hatchlings from fourth‐laid eggs showed lowest survival, even though hatchling mass tended to increase with hatch order. Survival of chicks subjected to major health interventions was 69% after 4 months. No differences in survival were found between different genders, hybrids and pure kaki, hand‐reared or parent‐reared birds, chicks hatching early or late in the season, different seasons, different‐sized groups of chicks, chicks reared in different brooders, juveniles kept in different aviaries, and chicks from subsequent clutches. Birds subjected to minor health interventions were equally likely to survive as healthy chicks (82%). Survival was high despite aggressive management (quadruple clutching and collecting late in the season). Differences between captive and wild birds suggest further improvements could be made to captive diet. Wide variation in hatchability between parent pairs substantiates the practice of breaking up poorly performing pairs. Zoo Biol 0:1–16, 2005. © 2005 Wiley‐Liss, Inc.