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Avian malaria is a disease caused by
species of protozoan parasites (Plasmodium)
that infect birds. Related species
commonly infect reptiles, birds and mammals
in tropical and temperate regions of
the world. Transmitted by mosquitoes,
the parasites spend part of their lives in
the red blood cells of birds (Figure 1).
Avian malaria is common in continental
areas, but is absent from the most isolated |
-tible to this disease. Malaria currently
limits the geographic distribution of native
species, has population level impacts
on survivorship, and is limiting the recovery
of threatened and endangered species
of forest birds. Altitudinal and Geographic Distribution of Avian Malaria Several factors influence the prevalence of avian malaria across the Hawaiian archipelago. Hawai¡®i has a wide spectrum of climatic zones and habitats that differ in rainfall, temperature and elevation. These habitats vary in their suitability for species that harbor and transmit malaria. Mosquitoes, for example, are more likely to be found in wet, low elevation habitats with temporary or permanent bodies of standing water that provide habitat for larval development. Similarly, infection rates among birds in the islands also differ due to differences in susceptibility and how well they overlap with suitable mosquito habitat. One of the most important developments since the 1970s is the emergence of recovering lowland populations of Hawai¡®i ¡®amakihi (Hemignathus virens) in the Puna District of Hawai¡®i Island. These birds have changed our view of how malaria is transmitted across the larger landscape on the eastern slopes of Kilauea Volcano |
 Figure 2. Our current understanding of the distribution of avian malaria on Mauna Loa and Kilauea Volcanoes after emergence of disease- resistant, low elevation Hawai‘i ‘amakihi populations. Disease prevalence (abundance) and transmission fall as elevation increases both because of thermal limits on development of the parasite in the vector and because mosquitoes decline in numbers and become more seasonal at higher altitudes. Populations of native birds at high elevation are more diverse and include the species that have little or no natural resistance to malaria. The absence of native birds at middle elevations is still incompletely understood and may reflect lower rates of natural selection for disease resistance that occur in areas with seasonal malarial transmission. A good test of this hypothesis will be to see if these areas are recolonized over the next decade by disease resistant ‘amakihi from the lowlands. | |
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Figure 1. Blood smear from an ‘apapane infected
with Plasmodium relictum. The parasites
(red arrows) develop within the circulating red
blood cells and stain purple. Red blood cell
nuclei (black arrows) in parasitized cells are
frequently pushed to one end of the cell. island archipelagos where mosquitoes do not naturally occur. More than 40 different species of avian Plasmodium have been described, but only one, P. relictum, has been introduced to the Hawaiian Islands. Because they evolved without natural exposure to avian malaria, native Hawaiian honeycreepers are extremely suscep- |
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| U.S. Department of the Interior U.S. Geological Survey |
USGS FS 2005-3151 December 2005 |
| (Figure 2). Their presence here and
elsewhere in Hawai'i indicates that some
native species have the capacity to evolve
resistance to this disease.
Malaria is most common at middle
(900¨C1500 m) elevations on moist, windward
sides of all of the main Hawaiian Islands
where native species still occur, but
has not been reported in the Northwestern
Hawaiian Islands. It is uncommon to
rare in alpine habitats on Mauna Loa,
Mauna Kea, and Haleakal'a Volcanoes
and is found almost entirely in birds that
have moved from lower elevations. Malaria
appears to be abundant in lowland
habitats in areas with recovering native
bird populations, but is less common in
areas that are dominated by non-native
species. The disease can be found in very
dry habitats, but generally only in areas
where mosquito populations are supported
by intermittent sources of water. Seasonal Transmission of Avian Malaria Malaria transmission becomes increasingly seasonal as elevation increases, both because numbers of mosquitoes are very low at higher elevations during the cooler winter months and because of thermal constraints on development of the parasite in the mosquito vector. Malaria transmission at elevations between 900 and 1500 m typically occurs during the warmest time of the year between September and December when mosquito populations reach their peak. This period follows the nesting season for most native species and the abundance of recently fledged, susceptible juvenile |
birds coupled with increasing mosquito
populations can lead to epidemic outbreaks
that may continue to the onset
of colder winter temperatures in January
(Figure 3). Transmission may occur
throughout the year at lower elevations if
suitable reservoir hosts and susceptible,
uninfected birds are present. Reservoirs of Infection Perhaps surprisingly, the highest prevalence of malaria and the highest intensity of infections now occur in highly susceptible native species (Figure 4). Malaria may have been introduced in a songbird or game bird species to which it was closely adapted. After initial spread to native forest birds, the source host may not have become established in the islands, leaving a parasite behind that was highly pathogenic (able to inflict  Figure 4. Prevalence of avian malaria in native and non-native species from mid-elevation habitats on the windward and leeward slopes of Mauna Loa Volcano. A. Kilauea Iki Crater, Hawai‘i Volcanoes National Park. B. Kona Unit, Hakalau Forest National Wildlife Refuge |
damage) in native birds, but with low
infectivity and pathogenicity to other
non-native species that became established
here. Alternatively, the source host
may be established in the islands, but
with a range that is more restricted than
the current distribution of avian malaria.
We do not know the original host species,
but one likely culprit is the House Sparrow
(Passer domesticus) which maintains
blood stage infections and infectiousness
to mosquito vectors for long periods of
time with no evidence of clinical signs.
Among native species, ‘apapane (Himatione
sanguinea) and ‘amakihi (Hemignathus
spp.) generally have the highest
prevalence of infection in the wild. Mortality in Native Forest Birds Experimental studies of the pathogenicity of avian malaria have been instrumental in documenting relative susceptibility and mortality among native and non-native species and documenting evidence of evolving resistance in some low elevation populations of Hawai'i 'amakihi (Hemignathus virens). Among species we have tested, both 'i'iwi (Vestiaria coccinea) and Maui 'alauahio (Paroreomyza montana) are particularly sensitive to malaria, with mortalities of 90% and 75%, respectively, following exposure to single infective mosquito bites. Both of these species rarely occur at elevations below 1200 m, suggesting that disease transmission may be a primary factor limiting their current distribution. By contrast, o ma o (Myadestes obscurus) and low elevation populations of Hawai'i 'amakihi from the Puna District are more capable of surviving infection, with little or no mortality after exposure to single infective mosquito bites. |
 Figure 3. Percent prevalence of avian malaria in hatch-year ‘apapane at Kilauea Iki Crater in Hawai‘i Volcanoes National Park between 1992 and 1998. Epidemic outbreaks at this mid- elevation (1200 m) site are limited to the warmer months of the year between September and December. Prevalence varies from year to year for a variety of reasons including variations in rainfall, vector populations, and numbers of susceptible juvenile birds. | Signs of Acute Malaria The earliest detectable evidence of malaria infection in highly susceptible honeycreepers is the appearance of parasites in circulating blood cells from 48 to 72 hours after exposure to an infective mosquito bite. Parasites begin rapid multiplication in the blood cells, but the first overt signs of infection do not begin until approximately seven days post-infection when declines in food consumption and activity levels first become evident. Among honeycreepers that eventually recover from infection, peak levels of parasites in the blood normally | ||
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| Figure 5. Characteristic signs and lesions of
acute malaria. A. Red blood cell destruction
and anemia is the primary cause of death in
acute infections. After tubes of whole blood
are spun in a centrifuge, volume of packed
red blood cells is significantly lower in a wild
‘apapane with acute malaria (left) than in an
uninfected canary. B. Lesions in an ‘i‘iwi with
acute malaria. Note enlarged, blackened liver
(arrow). C. Blood smear from an ‘i‘iwi with
acute malaria. Mature red blood cells have
been destroyed and replaced with immature
red blood cells and their precursors to compensate
for anemia caused by cell destruction.
D. Hawai‘i ‘amakihi with acute malaria. At the
crisis, birds become sedentary, cease feeding,
and may be very susceptible to predation. occur about 12 days post-infection when approximately 25% of the circulating red blood cells are infected. The crisis passes as the immune system begins to control numbers of parasites in the circulation. During the peak period of parasitemia or “crisis”, birds become sedentary and may cease feeding altogether. Among honeycreepers that succumb to infection, up to 80% of the circulating red blood cells may be parasitized. Most deaths occur between 18 and 24 days after infection and birds are typically from 20 to 40% below normal body weight |
and have a prominent sternum or “keel”.
Gross lesions are easy to recognize at
necropsy and include enlarged, chocolate
brown or black liver and spleen and thin,
watery blood (Figure 5). The most likely
cause of death is anemia associated with
destruction of red blood cells. Chronic Malaria and Problems with Disease Diagnosis Honeycreepers that survive acute malaria develop chronic, low level infections that may persist for the lifetime of the bird. Unlike acute infections, numbers of parasites in the peripheral circulation may be extremely low and difficult to detect by microscopy. Available experimental evidence indicates that these birds are immune to re-infection. They may exhibit no outward signs of being infected and may be in excellent body condition, yet are still infectious to mosquitoes and are excellent reservoir hosts for maintaining the disease in forest bird populations. |
Chronically infected birds may also carry
genes for disease resistance and may be
good candidates for translocation or captive
propagation for restoring forest bird
populations in locations where vector
control is not feasible. Accurate identification
of these individuals is important
when assessing disease risks for an area. Sensitivity and Specificity of Different Diagnostic Methods Both direct and indirect methods have been developed for diagnosing malaria. Direct methods that demonstrate the parasite or a portion of its DNA sequence include microscopy and polymerase chain reaction (PCR) techniques. Microscopy is still considered the “gold standard” for malaria diagnosis because parasites are actually seen within the blood cells, but it can miss more than 70% of chronic infections because numbers of parasites are so low. PCR methods that amplify specific portions of parasite DNA are significantly |
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| Figure 6. Examples of different diagnostic tests for avian malaria. A. ELISA (Enzyme-Linked Immunosorbant Assay) consists of a 96 well plate coated with malarial antigen and incubated sequentially with test plasma, enzyme-labeled antibodies and substrate. A positive test is indicated by the development of yellow color. Samples are typically run in triplicate. B. PCR (Polymerase Chain Reaction). Primers specific to portions of malarial ribosomal DNA are used to amplify short segments of DNA. These are separated on an agarose gel and stained with a dye that is visible under ultraviolet light. A positive test is indicated by presence of a band of the correct size. Lanes 1–17 are from sequential blood samples collected from the same bird over a two year period. Lanes +, 19 and 20 are positive and negative controls. C. Western blotting. Malarial proteins are separated into bands of different molecular weight on a polyacrylamide gel, transferred to a membrane and then incubated with test plasma, enzyme-labeled secondary antibodies and substrate. A positive test is indicated by the development of dark bands that correspond to malarial proteins of specific molecular weight. Each lane (1–5) was incubated with plasma from a different bird with known malarial infections. Lane C is a negative control. | |||
more sensitive than microscopy, but are
more expensive, time consuming and
may require additional sequencing steps
to confirm that the products originated
from parasite DNA.
Indirect methods for demonstrating
infection with malaria include serological
(blood) screening for the presence of antibodies
to the parasite. Two methods have
been applied to diagnosing avian malaria
in Hawai‘i: Enzyme Linked Immunosorbant
Assay (ELISA) and Western Blotting
(Figure 6) . ELISA is more sensitive than
Western Blotting, but may require additional
tests by Western Blotting to verify
positive results. Western Blotting is the
most specific serological test available for
avian malaria and can be used to verify
both ELISA and PCR tests.
Microscopy, serology and PCR can all
play important roles in providing accurate
diagnostic information about malarial
infections in Hawaiian birds. When used
alone, the tests vary in their ability to
accurately detect chronic malarial infections
with low intensities. Microscopy is
most likely to miss chronic infections, but
it is extremely accurate when parasites
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are detected and can be used to obtain
information on intensity of infection and
host cellular responses. Serological methods
are extremely sensitive for detecting
older infections in recovered birds because
persistent infections stimulate antibody
production and cellular immunity to
the parasite. They provide no information
about parasite intensity or morphology,
however, and are also likely to miss very
early acute infections, before the host is
able to produce antibodies to the parasite. Recommended Reading Atkinson, C.T., K.L. Woods, R.J. Dusek, L.S. Sileo and W.M. Iko. 1995. Wildlife disease and conservation in Hawaii: pathogenicity of avian malaria (Plasmodium relictum) in experimentally infected Iiwi (Vestiaria coccinea). Parasitology 111: S59–S69. Atkinson, C.T., R.J. Dusek and J.K. Lease. 2001. Serological responses and immunity to superinfection with avian malaria in experimentally-infected Hawaii Amakihi. Journal of Wildlife Diseases 37: 20–27. Jarvi, S.I., J.J. Schultz and C.T. Atkinson. 2002. PCR diagnostics underestimate the prevalence of avian malaria (Plasmodium relictum) in experimentally- infected passerines. Journal of Parasitology 88: 153–158. |
Available experimental evidence indicates
that PCR is not quite as sensitive
as serological methods for detecting
chronic infections, but it is much more
sensitive than microscopy. When used in
combination, these diagnostic methods
can complement each other and provide
critical information to resource managers
about the prevalence and distribution of
avian malaria in habitats that are being
considered for restoration of threatened
and endangered forest birds. van Riper III, C., S.G. van Riper, M.L. Goff and M. Laird. 1986. The epizootiology and ecological significance of malaria in Hawaiian landbirds. Ecological Monographs 56: 327–344. Woodworth, B.L., C.T. Atkinson, D.A. LaPointe, P.J. Hart, C.S. Spiegel, E.J. Tweed, C. Henneman, J. LeBrun, T. Denette, R. DeMots, K.L. Kozar, D. Triglia, D. Lease, A. Gregor, T. Smith, and D. Duffy. 2005. Host population persistence in the face of introduced vector-borne diseases: Hawaii ‘amakihi and avian malaria. Proceedings of the National Academy of Sciences, 102: 1531–1536. For more information contact: Carter T. Atkinson Phone: 808-967-8119, ext. 271 Email: Carter_Atkinson@usgs.govPhoto credits: All photos were taken by USGS researchers. |
U.S. Department of the Interior |
U.S. Geological Survey
URL: http://biology.usgs.gov/pierc/
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