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Changing climate and the altitudinal range of avian malaria in the Hawaiian Islands: an ongoing conservation crisis on the island of Kaua'i

Transmission of avian malaria in the Hawaiian Islands varies across altitudinal gradients and is greatest at elevations below 1500 m where both temperature and moisture are favorable for the sole mosquito vector, Culex quinquefasciatus, and extrinsic sporogonic development of the parasite, Plasmodium relictum. Potential consequences of global warming on this system have been recognized for over a decade with concerns that increases in mean temperatures could lead to expansion of malaria into habitats where cool temperatures currently limit transmission to highly susceptible endemic forest birds. Recent declines in two endangered species on the island of Kaua'i, the ‘Akikiki (Oreomystis bairdi) and ‘Akeke'e (Loxops caeruleirostris), and retreat of more common native honeycreepers to the last remaining high elevation habitat on the Alaka'i Plateau suggest that predicted changes in disease transmission may be occurring. We compared prevalence of malarial infections in forest birds that were sampled at three locations on the Plateau during 1994–1997 and again during 2007–2013, and also evaluated changes in the occurrence of mosquito larvae in available aquatic habitats during the same time periods. Prevalence of infection increased significantly at the lower (1100 m, 10.3% to 28.2%), middle (1250 m, 8.4% to 12.2%), and upper ends of the Plateau (1350 m, 2.0% to 19.3%). A concurrent increase in detections of Culex larvae in aquatic habitats associated with stream margins indicates that populations of the vector are also increasing. These increases are at least in part due to local transmission because overall prevalence in Kaua'i ‘Elepaio (Chasiempis sclateri), a sedentary native species, has increased from 17.2% to 27.0%. Increasing mean air temperatures, declining precipitation, and changes in streamflow that have taken place over the past 20 years are creating environmental conditions throughout major portions of the Alaka'i Plateau that support increased transmission of avian malaria.

Hawai'i

Adherence of Myxobolus cerebralis myxospores to waders: Implications for disease dissemination

The vectors involved in the spread of whirling disease, which is caused by Myxobolus cerebralis, are only partly understood. However, the parasite has rapidly become established in many regions, suggesting that it is easily disseminated. We gained insight into transport vectors by examining the surface porosity of common wading equipment materials and the adherence of M. cerebralis myxospores to them. Interstitial spaces within rubber, felt, lightweight nylon, and neoprene were measured on scanning electron microscope images. Myxospores were applied to each material, the material was rinsed, and the myxospores recovered to assess adherence. The mean interstitial space size of rubber was the smallest (2.0 ??m), whereas that of felt was the largest (31.3 ??m). The highest recovery rates were from rubber and the glass control. Percent myxospore recovery varied by material, the recovery from felt being lower than that from all other materials. The potential for felt to carry even small numbers of myxospores suggests that the introduction of M. cerebralis by felt-soled wading boots is possible. ?? Copyright by the American Fisheries Society 2008.

North American Journal of Fisheries Management

Characterization of Plasmodium relictum, a cosmopolitan agent of avian malaria

Background Microscopic research has shown that Plasmodium relictum is the most common agent of avian malaria. Recent molecular studies confirmed this conclusion and identified several mtDNA lineages, suggesting the existence of significant intra-species genetic variation or cryptic speciation. Most identified lineages have a broad range of hosts and geographical distribution. Here, a rare new lineage of P. relictum was reported and information about biological characters of different lineages of this pathogen was reviewed, suggesting issues for future research. Methods The new lineage pPHCOL01 was detected in Common chiffchaff Phylloscopus collybita, and the parasite was passaged in domestic canaries Serinus canaria . Organs of infected birds were examined using histology and chromogenic in situ hybridization methods. Culex quinquefasciatus mosquitoes, Zebra finch Taeniopygia guttata, Budgerigar Melopsittacus undulatus and European goldfinch Carduelis carduelis were exposed experimentally. Both Bayesian and Maximum Likelihood analyses identified the same phylogenetic relationships among different, closely-related lineages pSGS1, pGRW4, pGRW11, pLZFUS01, pPHCOL01 of P. relictum. Morphology of their blood stages was compared using fixed and stained blood smears, and biological properties of these parasites were reviewed. Results Common canary and European goldfinch were susceptible to the parasite pPHCOL01, and had markedly variable individual prepatent periods and light transient parasitaemia. Exo-erythrocytic and sporogonic stages were not seen. The Zebra finch and Budgerigar were resistant. Neither blood stages nor vector stages of all examined P. relictum lineages can be distinguished morphologically. Conclusion Within the huge spectrum of vertebrate hosts, mosquito vectors, and ecological conditions, different lineages of P. relictum exhibit indistinguishable, markedly variable morphological forms. Parasites of same lineages often develop differently in different bird species. Even more, the variation of biological properties (parasitaemia dynamics, blood pathology, prepatent period) in different isolates of the same lineage might be greater than the variation in different lineages during development in the same species of birds, indicating negligible taxonomic value of such features. Available lineage information is excellent for parasite diagnostics, but is limited in predictions about relationships in certain host-parasite associations. A combination of experiments, field observations, microscopic and molecular diagnostics is essential for understanding the role of different P. relictum lineages in bird health.

Malaria Journal

Towards common ground in the biodiversity–disease debate

The disease ecology community has struggled to come to consensus on whether biodiversity reduces or increases infectious disease risk, a question that directly affects policy decisions for biodiversity conservation and public health. Here, we summarize the primary points of contention regarding biodiversity–disease relationships and suggest that vector-borne, generalist wildlife and zoonotic pathogens are the types of parasites most likely to be affected by changes to biodiversity. One synthesis on this topic revealed a positive correlation between biodiversity and human disease burden across countries, but as biodiversity changed over time within these countries, this correlation became weaker and more variable. Another synthesis—a meta-analysis of generally smaller-scale experimental and field studies—revealed a negative correlation between biodiversity and infectious diseases (a dilution effect) in various host taxa. These results raise the question of whether biodiversity–disease relationships are more negative at smaller spatial scales. If so, biodiversity conservation at the appropriate scales might prevent wildlife and zoonotic diseases from increasing in prevalence or becoming problematic (general proactive approaches). Further, protecting natural areas from human incursion should reduce zoonotic disease spillover. By contrast, for some infectious diseases, managing particular species or habitats and targeted biomedical approaches (targeted reactive approaches) might outperform biodiversity conservation as a tool for disease control. Importantly, biodiversity conservation and management need to be considered alongside other disease management options. These suggested guiding principles should provide common ground that can enhance scientific and policy clarity for those interested in simultaneously improving wildlife and human health.

Nature Ecology & Evolution

Spring viremia of carp

pring viremia of carp (SVC) is an important disease affecting cyprinids, mainly common carp Cyprinus carpio . The disease is widespread in European carp culture, where it causes significant morbidity and mortality. Designated a notifiable disease by the Office International des Epizooties, SVC is caused by a rhabdovirus, spring viremia of carp virus (SVCV). Affected fish show destruction of tissues in the kidney, spleen and liver, leading to hemorrhage, loss of water-salt balance and impairment of immune response. High mortality occurs at water temperatures of 10 to 17°C, typically in spring. At higher temperatures, infected carp develop humoral antibodies that can neutralize the spread of virus and such carp are protected against re-infection by solid immunity. The virus is shed mostly with the feces and urine of clinically infected fish and by carriers. Waterborne transmission is believed to be the primary route of infection, but bloodsucking parasites like leeches and the carp louse may serve as mechanical vectors of SVCV. The genome of SVCV is composed of a single molecule of linear, negative-sense, single-stranded RNA containing 5 genes in the order 3¹-NPMGL-5¹ coding for the viral nucleoprotein, phosphoprotein, matrix protein, glycoprotein, and polymerase, respectively. Polyacrylamide gel electrophoresis of the viral proteins, and sequence homologies between the genes and gene junctions of SVCV and vesicular stomatitis viruses, have led to the placement of the virus as a tentative member of the genus Vesiculovirus in the family Rhabdoviridae . These methods also revealed that SVCV is not related to fish rhabdoviruses of the genus Novirhabdovirus . In vitro replication of SVCV takes place in the cytoplasm of cultured cells of fish, bird and mammalian origin at temperatures of 4 to 31°C, with an optimum of about 20°C. Spring viremia of carp can be diagnosed by clinical signs, isolation of virus in cell culture and molecular methods. Antibodies directed against SVCV react with the homologous virus in serum neutralization, immunofluorescence, immunoperoxidase, or enzyme-linked immunosorbent assays, but they cross-react to various degrees with the pike fry rhabdovirus (PFR), suggesting the 2 viruses are closely related. However, SVCV and PFR can be distinguished by certain serological tests and molecular methods such as the ribonuclease protection assay.

Diseases of Aquatic Organisms

The Ozobranchus leech is a candidate mechanical vector for the fibropapilloma-associated turtle herpesvirus found latently infecting skin tumors on Hawaiian green turtles (Chelonia mydas)

Fibropapillomatosis (FP) of marine turtles is a neoplastic disease of ecological concern. A fibropapilloma-associated turtle herpesvirus (FPTHV) is consistently present, usually at loads exceeding one virus copy per tumor cell. DNA from an array of parasites of green turtles ( Chelonia mydas ) was examined with quantitative PCR (qPCR) to determine whether any carried viral loads are sufficient to implicate them as vectors for FPTHV. Marine leeches ( Ozobranchus spp.) were found to carry high viral DNA loads; some samples approached 10 million copies per leech. Isopycnic sucrose density gradient/qPCR analysis confirmed that some of these copies were associated with particles of the density of enveloped viruses. The data implicate the marine leech Ozobranchus as a mechanical vector for FPTHV. Quantitative RT-PCR analysis of FPTHV gene expression indicated that most of the FPTHV copies in a fibropapilloma have restricted DNA polymerase expression, suggestive of latent infection.

Florida, Hawai'i

Tick-, mosquito-, and rodent-borne parasite sampling designs for the National Ecological Observatory Network

Parasites and pathogens are increasingly recognized as significant drivers of ecological and evolutionary change in natural ecosystems. Concurrently, transmission of infectious agents among human, livestock, and wildlife populations represents a growing threat to veterinary and human health. In light of these trends and the scarcity of long-term time series data on infection rates among vectors and reservoirs, the National Ecological Observatory Network (NEON) will collect measurements and samples of a suite of tick-, mosquito-, and rodent-borne parasites through a continental-scale surveillance program. Here, we describe the sampling designs for these efforts, highlighting sampling priorities, field and analytical methods, and the data as well as archived samples to be made available to the research community. Insights generated by this sampling will advance current understanding of and ability to predict changes in infection and disease dynamics in novel, interdisciplinary, and collaborative ways.

Ecosphere

First record of the non-indigenous parasitic copepod Neoergasilus japonicus (Harada, 1950) in the Lake Ontario Watershed: Oneida Lake, New York

Four specimens of the Asiatic parasitic copepod Neoergasilus japonicus (Harada, 1930) were collected from Oneida Lake, New York in September 2018; one specimen was from a white sucker Catostomus commersonii , another from a green sunfish Lepomis cyanellus , and two from a bluegill Lepomis macrochirus . The four adult female specimens were found attached to the base of the gills of their respective hosts along with other ergasilid species. The average total length of the adult female N. japonicus specimens we found was 0.609 mm. These detections represent the first known occurrence of this non-native species in the state of New York, extends the easternmost distribution of this parasite over 400 miles, and now includes the Lake Ontario watershed for the first time. It is commonly believed that the international aquaculture industry and aquarium fish trade are the most likely vectors of dispersal for N. japonicus . Monitoring the spread of non-indigenous aquatic species is an important step towards the development of management plans and mitigation efforts with regards to the anthropogenic causes of dispersal, and fish parasites are no exception.

New York

Mapping the distribution of malaria: current approaches and future directions

Mapping the distribution of malaria has received substantial attention because the disease is a major source of illness and mortality in humans, especially in developing countries. It also has a defined temporal and spatial distribution. The distribution of malaria is most influenced by its mosquito vector, which is sensitive to extrinsic environmental factors such as rainfall and temperature. Temperature also affects the development rate of the malaria parasite in the mosquito. Here, we review the range of approaches used to model the distribution of malaria, from spatially explicit to implicit, mechanistic to correlative. Although current methods have significantly improved our understanding of the factors influencing malaria transmission, significant gaps remain, particularly in incorporating nonlinear responses to temperature and temperature variability. We highlight new methods to tackle these gaps and to integrate new data with models.

Book chapter

Avian haematozoa 3. Color atlas of leucocytozoon simondi

The life cycle of Leucocytozoon simondi is Illustrated in a series of color photomicrographs of the various stages of development in the blackfly vector and in the tissues and blood of Anatidae. A brief discussion of the life cycle is presented and taxonomic status of the parasite is reviewed. The bibliography includes references to the stages depicted and other phases of the development, morphology and pathogenesis of .L. simondi.

Wildlife Disease

Waterfowl endozoochory: An overlooked long-distance dispersal mode for Cuscuta (dodder)

REMISE OF THE STUDY: Dispersal of parasitic Cuscuta species (dodders) worldwide has been assumed to be largely anthropomorphic because their seeds do not match any previously known dispersal syndrome and no natural dispersal vectors have been reliably documented. However, the genus has a subcosmopolitan distribution and recent phylogeographic results have indicated that at least18 historical cases of long-distance dispersal (LDD) have occurred during its evolution. The objective of this study is to report the first LDD biological vector for Cuscuta seeds. METHODS: Twelve northern pintails ( Anas acuta ) were collected from Suisun Marsh, California and the contents of their lowest part of the large intestine (rectum) were extracted and analyzed. Seed identification was done both morphologically and using a molecular approach. Extracted seeds were tested for germination and compared to seeds not subjected to gut passage to determine the extent of structural changes caused to the seed coat by passing through the digestive tract. KEY RESULTS: Four hundred and twenty dodder seeds were found in the rectum of four northern pintails. From these, 411 seeds were identified as Cuscuta campestris and nine as most likely C. pacifica . The germination rate of C. campestris seeds after gut passage was 55%. Structural changes caused by the gut passage in both species were similar to those caused by an acid scarification. CONCLUSIONS: Endozoochory by waterbirds may explain the historical LDD cases in the evolution of Cuscuta . This also suggests that current border quarantine measures may be insufficient to stopping spreading of dodder pests along migratory flyways.

American Journal of Botany

Studies on avian malaria in vectors and hosts of encephalitis in Kern County, California. I. Infections in avian hosts

An epizoological study of Plasmodium infections in wild birds of Kern County, California, in the years 1946 through 1951 greatly extended knowledge of the occurrence of these parasites and their behavior in nature. Examination of 10,459 blood smears from 8,674 birds representing 73 species resulted in the observation of Plasmodium spp. in 1,094 smears representing 888 individual birds of 27 species. Seven species of Plasmodium were found: relictum, elongatum, hexamerium, nucleophilum, polare, rouxi and vaughani. Plasmodium relictum was by far the most frequently observed species, occurring in at least 79 per cent of the infected birds. Twelve new host species are recorded for this parasite. Sufficient morphological variation was observed to indicate that two strains of this species probably exist in nature. Numerous new host records were made of plasmodia with elongate gametocytes. The finding of parasites believed to be P. rouxi in two new host species represents the first record of the occurrence of this Plasmodium outside of Algeria. Multiple smears were obtained from a number of individual birds over varying time periods. Evidence of prolonged parasitemia was unusual, but some individuals had parasitemia on consecutive months and even for three successive years. In most individuals, parasitemias were of short duration. The inoculation of blood from wild birds into canaries led to the demonstration of many infections not observed on blood smear examination of donors. Use of these two complementary techniques led to more complete host records and a truer picture of the prevalence of infection. Three age classes of birds were studied--nestling, immature (less than 1 year of age) and adult. Parasites were observed in all three groups but infections in the younger individuals were most susceptible to interpretation. As to time of onset, numerous records were obtained of infection in nestling birds. Prevalence rates in immature birds after a single season's exposure ranged from 64 to 100 per cent in the house finch and 17 to 68 per cent in the English sparrow in different areas and years. Marked differences were found in the prevalence rates in different summer months, years and areas. It is believed these differences reflect variation in a number of environmental factors. This study indicates the extensive distribution of Plasmodium infection in a wide range of wild avian hosts. The observations are of possible importance in epidemiological studies of other arthropod-borne diseases such as the viral encephalitides for which these birds serve as hosts.

California

Juvenile i`iwi detected in lower elevations of Hawaii Volcanoes National Park

The Hawaiian islands are home to a diverse array of plants and animals found nowhere else on Earth. Among the most famous of these are the spectacular Hawaiian honeycreepers, a group that evolved from a single flock of ancestral finches into at least 54 unique species. Unfortunately, the same isolation that fostered such dramatic adaptive radiation left Hawaiian species vulnerable. Under the onslaught of alien species predation and competition, habitat degradation, and introduced infectious diseases and parasites, most of the surviving honeycreepers have become largely confined to higher elevations. Intact habitat exists above the warm-weather range of deadly introduced avian malaria ( Plasmodium relictum ), and its mosquito vector ( Culex quinquefasciatus ).

Hawai'i

Analysis of the trap gene provides evidence for the role of elevation and vector abundance in the genetic diversity of Plasmodium relictum in Hawaii

Background: The avian disease system in Hawaii offers an ideal opportunity to investigate host-pathogen interactions in a natural setting. Previous studies have recognized only a single mitochondrial lineage of avian malaria (Plasmodium relictum) in the Hawaiian Islands, but cloning and sequencing of nuclear genes suggest a higher degree of genetic diversity. Methods: In order to evaluate genetic diversity of P. relictum at the population level and further understand host-parasite interactions, a modified single-base extension (SBE) method was used to explore spatial and temporal distribution patterns of single nucleotide polymorphisms (SNPs) in the thrombospondin-related anonymous protein (trap) gene of P. relictum infections from 121 hatch-year amakihi (Hemignathus virens) on the east side of Hawaii Island. Results: Rare alleles and mixed infections were documented at three of eight SNP loci; this is the first documentation of genetically diverse infections of P. relictum at the population level in Hawaii. Logistic regression revealed that the likelihood of infection with a rare allele increased at low-elevation, but decreased as mosquito capture rates increased. The inverse relationship between vector capture rates and probability of infection with a rare allele is unexpected given current theories of epidemiology developed in human malarias. Conclusions: The results of this study suggest that pathogen diversity in Hawaii may be driven by a complex interaction of factors including transmission rates, host immune pressures, and parasite-parasite competition.

Hawai'i

The rise and fall of infectious disease in a warmer world

Now-outdated estimates proposed that climate change should have increased the number of people at risk of malaria, yet malaria and several other infectious diseases have declined. Although some diseases have increased as the climate has warmed, evidence for widespread climate-driven disease expansion has not materialized, despite increased research attention. Biological responses to warming depend on the non-linear relationships between physiological performance and temperature, called the thermal response curve. This leads performance to rise and fall with temperature. Under climate change, host species and their associated parasites face extinction if they cannot either thermoregulate or adapt by shifting phenology or geographic range. Climate change might also affect disease transmission through increases or decreases in host susceptibility and infective stage (and vector) production, longevity, and pathology. Many other factors drive disease transmission, especially economics, and some change in time along with temperature, making it hard to distinguish whether temperature drives disease or just correlates with disease drivers. Although it is difficult to predict how climate change will affect infectious disease, an ecological approach can help meet the challenge.

F1000 Research

A comparison of avian hematozoan epizootiology in two California coastal scrub communities

Passerine birds within two California (USA) coastal scrub ecosystems, an island and a mainland site, were examined for hematozoa from 1984 to 1990. Island birds had a significantly lower hematozoan prevalence than mainland birds. This prevalence difference can be related to a lack of appropriate hematozoan vectors on the island. Haemoproteus spp. and Leucocytozoon spp. were the most commonly encountered hematozoa; four new species of Leucocytozoon spp. and one new Haemoproteus sp. were found in five host families. No transmission of hematozoan parasites was detected at the island site during the study. At the mainland coastal scrub site, Leucocytozoon spp. was transmitted each year while Plasmodium spp. and Haemoproteus spp. transmission varied between years. There was evidence that some species of birds acquired infections outside of their breeding season. Results of this study lend further support to the prediction of decreased disease on remote island ecosystems.

Journal of Wildlife Diseases

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. ?? American Society of Parasitologists 2005.

Journal of Parasitology

Ecology and conservation biology of avian malaria

Avian malaria is a worldwide mosquito-borne disease caused by Plasmodium parasites. These parasites occur in many avian species but primarily affect passerine birds that have not evolved with the parasite. Host pathogenicity, fitness, and population impacts are poorly understood. In contrast to continental species, introduced avian malaria poses a substantial threat to naive birds on Hawaii, the Galapagos, and other archipelagoes. In Hawaii, transmission is maintained by susceptible native birds, competence and abundance of mosquitoes, and a disease reservoir of chronically infected native birds. Although vector habitat and avian communities determine the geographic distribution of disease, climate drives transmission patterns ranging from continuous high infection in warm lowland forests, seasonal infection in midelevation forests, and disease-free refugia in cool high-elevation forests. Global warming is expected to increase the occurrence, distribution, and intensity of avian malaria across this elevational gradient and threaten high-elevation refugia, which is the key to survival of many susceptible Hawaiian birds. Increased temperatures may have already increased global avian malaria prevalence and contributed to an emergence of disease in New Zealand.

Hawai'i