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Avian malaria

Avian malariais aparasitic diseaseof birds, caused by parasite species belonging to the generaPlasmodiumandHemoproteus(phylumApicomplexa,class Haemosporidia, family Plasmoiidae).[1]The disease is transmitted by a dipteranvectorincludingmosquitoesin the case ofPlasmodiumparasites andbiting midgesforHemoproteus.The range of symptoms and effects of the parasite on its bird hosts is very wide, from asymptomatic cases to drastic population declines due to the disease, as is the case of theHawaiian honeycreepers.[2]The diversity of parasites is large, as it is estimated that there are approximately as many parasites as there are species of hosts. As research on human malaria parasites became difficult, Dr. Ross studied avian malaria parasites.[3]Co-speciationand host switching events have contributed to the broad range of hosts that these parasites can infect, causing avian malaria to be a widespread global disease, found everywhere except Antarctica.

Cause

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Avian malaria is most notably caused byPlasmodium relictum,aprotistthat infects birds in all parts of the world apart from Antarctica. Captive penguins in non-native environments are exposed to the protozoa without having coevolved with them and are especially sensitive to infection. The most common presentation of the disease in affected penguins is acute death. Infection of wild penguins is reported and a greater understanding of the significance of such infections is required.[4]There are several otherspeciesofPlasmodiumthat infect birds, such asPlasmodium anasumandPlasmodium gallinaceum,but these are of less importance except, in occasional cases, for thepoultryindustry. The disease is found worldwide, with important exceptions.[5]Usually, it does not kill birds. However, in areas where avian malaria is newly introduced, such as the islands of Hawaiʻi, it can be devastating to birds that have lost evolutionary resistance over time, like the Mohoidae family.

Parasite species

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Avian malaria is avector-transmitteddisease caused byprotozoain the generaPlasmodiumandHaemoproteus;these parasites reproduceasexuallywithin bird hosts and both asexually and sexually within their insect vectors, which include mosquitoes (Culicidae), biting midges (Ceratopogonidae), and louse flies (Hippoboscidae).[6]The blood-parasites of the genusPlasmodiumandHaemoproteus,encompass an extremely diverse group of pathogens with global distribution.[7]The large number ofparasite lineagesalong with their wide range of potential host species and the pathogen's capacity for host switching makes the study of this system extremely complex.[1]Evolutionary relationships between hosts and the parasites have only added complexity and suggested extensive sampling is needed to elucidate how global cospeciation events drive disease transmission and maintenance in various ecosystems.[8]In addition to this, the parasite's ability to disperse can be mediated bymigratory birdsand thus increases variation inprevalencepatterns and alters host-parasite adaptation processes.[9]Host susceptibility is highly variable as well and numerous efforts have been made to understand the relationship between increased prevalence and host traits such as nesting and foraging height,sexual dimorphismor evenincubationtime length. So far, the effects of this disease in wild populations is poorly understood. A 2015 study using blood samples fromMalawianbird fauna found that close to 80% of were infected with either malaria or closely relatedalveolates.Closed-cup nesters, such asweaversandCisticola,were more likely to be infected with Plasmodium than with midge-borne parasites such as Haemoproteus andLeucocytozoon.[10]

There exists much controversy on what corresponds as a species in avian malaria parasites. The Latin binomials nomenclature used to describePlasmodiumandHemoproteusparasites is based on a restricted set ofmorphological characteristicsand the restriction to which parasites of birds they are able to infect.[8]Therefore, considering co-speciation events or even speciesdiversityfor malaria parasites is surrounded by much disagreement. Molecular tools have directed classification towards a phylogenetic definition of lineages, based on sequence divergence and the range of hosts in which the parasite can be found. The diversity of avian malaria parasites and other haemosporidia is extremely large, and previous studies have found that the number of parasites approximates the number of hosts, with significant host switching events and parasite sharing.[1]The current approach suggests amplification of thecytochrome bgene of the parasite and the reconstruction of genealogies based on this information. Due to the large number of lineages and different host species, a public database called MalAvi has been created to encourage sharing these sequences and aid in understanding the diversity of these parasites.[11]Considering that no othergenetic markershave been developed for this group of parasites, a ~1.2-4% sequence divergence has been determined as a cutoff value to distinguish between different parasite lineages.[8]The molecular approach has also allowed direct comparisons between host phylogenies and parasite genealogies, and significant co-speciation has been found based on event-based-matching of phylogenetic trees.[citation needed]

Phylogeny of malaria parasites

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There is no specific phylogeny for avianmalaria parasitesand relatedhaemosporidianparasites. However, given that malaria parasites can be found in reptiles, birds and mammals, it is possible to combine the data from these groups and a well resolved largephylogenyis available.[12]For over a century, parasitologists classified malaria parasites based on morphological and life-history traits and new molecular data shows that these have variable phylogenetic signals. The current approach suggests thatPlasmodiumspecies infecting birds and squamate reptiles belong to one clade, and mammalian lineages belonging to a separate clade. In the case ofHaemoproteus,this group has traditionally been classified based on the vector host, with one clade being transmitted to columbiform birds byhippoboscid fliesand a second group transmitted bybiting midgesto other avian families. The molecular data supports this approach and suggests reclassifying the later group asParahaemoproteous.[citation needed]

Phylogeography of avian malaria

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Although a widespread disease, the culprit most commonly associated with the disease isPlasmodium relictumand associated lineages.To better understand the parasite's epidemiology and geographical distribution, analysis of genetic variation across large geographical scales have been conducted by looking at the nuclear gene MSP1 (merozoitesurface protein) fromPlasmodium relictum[13].Findings have revealed that there are significant differences between lineages from the New and Old World, suggesting different introductions of the parasite to avian populations. In addition to this, considerable variation was found between Europe and African lineages, suggesting different patterns of transmission for temperate and tropical populations. Although this approach is relatively recent, detecting allelic variation in different markers is essential to unveil parasite transmission patterns and the likelihood of introduction to new susceptible host populations.[citation needed]

Vector

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Contrary to the state of knowledge on parasite-avian interactions, parasite-vector relationships are relatively less explored. MalAvi[14]does list several known vectors however as of 2015this is not at all complete. Generally avian malaria organisms are vectored byCulex.[15]

Itsvectorin Hawaiʻi is themosquitoCulex quinquefasciatus,which wasintroducedto theHawaiian Islandsin 1826. Since then, avian malaria andavipoxvirustogether have devastated the native bird population, resulting in many extinctions. Hawaiʻi has more extinct birds than anywhere else in the world; just since the 1980s, ten unique birds have disappeared.[citation needed]

Virtually every individual of susceptibleendemicspecies below 4,000 feet (1,200 m) in elevation has been eliminated by the disease. These mosquitoes are limited to lower elevations, below 5,000 feet (1,500 m), by cold temperatures that prevent larval development. However, they appear to be slowly gaining a foothold at higher elevations and their range may be expanding upwards.[16]If so, most remaining Hawaiian land birds may become at risk to extinction.[citation needed]

Most of the Hawaiian Islands have a maximum elevation of less than 5,000 feet (1,500 m), so with the exception of theisland of HawaiʻiandEast Maui,native birds may becomeextincton every other island if the mosquito is able to occupy higher elevations.[citation needed]

Research on avian malaria

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Ronald Ross

Ronald Ross was born in Almora, India in 1857. Although he had no predisposition to medicine, at the age of 17 he submitted to his father’s wish to see him enter the Indian Medical Service. He began his medical studies atSt. Bartholomew’s Hospital Medical College,London in 1874 and sat the examinations for the Royal College of Surgeons of England in 1879. He took the post of ship surgeon on a transatlantic steamship while studying for, and gaining theLicentiate of the Society of Apothecaries,which allowed him to enter the Indian Medical Service in 1881, where he held temporary appointments in Madras, Burma, and the Andaman Islands. In 1892 he became interested in malaria and, having originally doubted the parasites’ existence, became an enthusiastic convert to the belief that malaria parasites were in the blood stream when this was demonstrated to him by Patrick Manson during a period of home leave in 1894.

In 1895, Ross embarked on a quest to prove the hypothesis of Alphonse Laveran and Manson[17]that mosquitoes were intricately linked to the propagation of malaria. On 20 August 1897, Ross made his landmark discovery in Secunderabad. While dissecting the stomach tissue of an anopheline mosquito that had fed on a patient with malaria four days earlier, he found the malaria parasite, thus conclusively proving the role ofAnophelesmosquitoes in the transmission of malaria parasites in humans. He continued his research into malaria in India, using a more convenient experimental model—malaria in birds. In 1898, he had demonstrated that mosquitoes could serve as intermediate hosts for bird malaria. After feeding mosquitoes on infected birds, he observed that malaria parasites could develop in the mosquitoes and migrate to the insects’ salivary glands, enabling the mosquitoes to infect other birds during subsequent blood meals.[18]In 1902, Ross was awarded the Nobel Prize in Medicine for his discovery of the mosquito transmission of malaria.[19]

Cycle of infection

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The infection cycle typically commences with immature parasites known as sporozoites, which are carried in the saliva of infected female mosquitoes, in variousPlasmodiumspecies. After being bitten by one of these mosquitoes, sporozoites either directly enter the bloodstream or deeply penetrate into the bird's skin, invadingfibroblastsandmacrophagesand maturing into forms calledmerozoites.Within 36 to 48 hours, merozoites are released into the bloodstream and transported to macrophages in the brain, liver, spleen, kidney, and lung. Subsequently, the parasites commenceasexual reproduction,generating copies of themselves. The new generations of merozoites infect red blood cells, where they grow, reproduce, and eventually cause the cells to burst open. This sudden release of parasites and the loss of red cells trigger the acute phase of infection. In susceptible birds, this phase is primarily characterized byanemia,accompanied by symptoms of weakness, depression, and loss of appetite. Some birds may even become comatose and die.[20]

Disease process and epidemiology

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Plasmodium relictumreproduces inred blood cells.If the parasite load is sufficiently high, the bird begins losing red blood cells, causinganemia.[21]Because red blood cells are critical for movingoxygenabout the body, loss of these cells can lead to progressive weakness and, eventually, death.[21]Malaria mainly affectspasserines(perching birds). In Hawaiʻi, this includes most of the nativeHawaiian honeycreepersand theHawaiian crow.Susceptibilityto the disease varies between species, for example, theʻiʻiwiis very susceptible to malaria while theʻApapaneless so.[21]Native Hawaiʻian birds are more susceptible than introduced birds to the disease and exhibit a highermortality rate(Van Riper et al. 1982; Atkinson et al. 1995). This has serious implications for native birdfaunas(SPREP) with P. relictum being blamed for therangerestriction and extinctions of a number of bird species in Hawaiʻi, primarilyforestbirds of low-land forestshabitatswhere the mosquito vector is most common.[22]

The incidence of this disease has nearly tripled in the last 70 years. Notable among the species of birds most heavily affected werehouse sparrows,great tits,andEurasian blackcaps.Prior to 1990, when global temperatures were cooler than now, less than 10 percent of house sparrows (Passer domesticus) were infected with malaria. In recent years, however, this figure has increased to nearly 30 percent. Likewise, since 1995, the percent of malaria-infected great tits has risen from 3 percent to 15 percent. In 1999, some 4 percent of blackcaps—a species once unaffected by avian malaria—were infected. For tawny owls in the UK, the incidence had risen from two or three percent to 60%.[23]

Although new epidemics are expected to be driven byspeciationevents the real situation is still poorly understood. Ellis et al 2015 findhost switchingis more common in avianhaemosporidiansincluding avian malaria organisms. They find secondary importance goes toadaptationto whateverhostpopulations are locally available.[24]

Control

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The main way to control avian malaria is to control mosquito populations. Hunting and removing pigs helps, because wallows fromferal pigsand hollowed out logs of the native hapu'u ferns providedirty standing waterwhere the mosquito breeds (USDI and USGS 2005). Around houses, reducing the number of potential water catchment containers helps reduce the mosquito breeding sites (SPREP Undated). However, in Hawaiʻi, attempts to control the mosquitoes bylarvalhabitat reduction andlarvicideuse have not eliminated the threat.[citation needed]

It may also be possible to find birds that are resistant to malaria, collect eggs and raise young birds for re-introduction into areas where birds are not resistant, giving the species a head-start on spreading resistance. There is evidence for evolution of resistance to avian malaria in two endemic species,Oʻahu ʻamakihiandHawaiʻi ʻamakihi.If other species can be preserved for long enough, they may evolve resistance as well. One tactic would be to reforest high-elevation areas on the island of Hawaiʻi, for example above the refuge of Hakalau on land managed by the Department of Hawaiʻian Homelands. This could give birds more time to adapt before climate change or mosquito evolution bring avian malaria to the last remaining bird populations.[citation needed]

Extirpatingmosquitos from Hawai'i usingCRISPRediting has also been suggested.[25]

Anti-Microbiota Vaccine Reduces Avian Malaria Infection Within Mosquito Vectors. The vector microbiome can be assembled in different possible states, some of which may be incompatible with pathogen infection and/or transmission, while others increase vector competence or could increase or reduce vector fitness. Unraveling how to modulate these different states in a precise manner offers a powerful tool to develop novel transmission-blocking vaccines. The results support the use of anti-microbiotavaccines to target vector commensal bacteria that facilitate pathogen infection. In addition totaxon-specific effects, the community-level effects and cascading ecological impact of anti-microbiota vaccines on vector microbiota might induce infection-refractory states in the vector microbiome. Effective infection by vector-borne pathogens involves competent vectors, infective pathogens, and an infection-compatible microbiome. Mismatch of at least one of these components can result in an impaired ability of the vector to support the pathogen life cycle. For example, one strategy used to reduce the vector competence for pathogens is the genetic modification of insects that no longer transmit pathogens. The results provide strong evidence that alterations in the vector midgut microbiomes, without the need to altering vector and/or pathogen genetics, affect pathogen infection in the vector. Therefore, deviations from infection-compatible microbiomes could block transmission and disease development. Anti-microbiota vaccines can be used as a microbiome manipulation tool for the induction of infection-refractory states in the vector microbiome for the control of major vector-borne pathogens such as malaria.

References

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  1. ^abcRicklefs, R. E.; Fallon, S. M. (2002-05-07)."Diversification and host switching in avian malaria parasites".Proceedings of the Royal Society of London B: Biological Sciences.269(1494): 885–892.doi:10.1098/rspb.2001.1940.ISSN0962-8452.PMC1690983.PMID12028770.
  2. ^van Riper, Charles; van Riper, Sandra G.; Goff, M. Lee; Laird, Marshall (1986-02-01). "The Epizootiology and Ecological Significance of Malaria in Hawaiian Land Birds".Ecological Monographs.56(4): 327–344.Bibcode:1986EcoM...56..327V.doi:10.2307/1942550.ISSN1557-7015.JSTOR1942550.
  3. ^Yoeli, M. (1973)."Sir Ronald Ross and the evolution of malaria research".Bulletin of the New York Academy of Medicine.49(8): 722–735.PMC1807077.PMID4580853.
  4. ^Ings, K.; Denk, D. (2022)."Avian Malaria in Penguins: Diagnostics and Future Direction in the Context of Climate Change".Animals.12(5): 600.doi:10.3390/ani12050600.PMC8909384.PMID35268169.
  5. ^Clark, Nicholas; Clegg, S.; Lima, M. (2014). "A review of global diversity in avian haemosporidians (Plasmodium and Haemoproteus: Haemosporida): new insights from molecular data".International Journal for Parasitology.44(5): 329–338.doi:10.1016/j.ijpara.2014.01.004.hdl:10072/61114.PMID24556563.
  6. ^Gediminas, Valkiunas (2005-01-01).Avian malarial parasites and other haemosporidia.Taylor & Francis.ISBN9780415300971.OCLC476614868.
  7. ^Bensch, Staffan; Pérez-Tris, Javier; Waldenström, Jonas; Hellgren, Olof; Poulin, R. (2004-07-01). "Linkage between nuclear and mitochondrial dna sequences in avian malaria parasites: multiple cases of cryptic speciation?".Evolution.58(7): 1617–1621.doi:10.1554/04-026.ISSN0014-3820.PMID15341164.S2CID198154866.
  8. ^abcRICKLEFS, ROBERT; FALLON, SYLVIA; BERMINGHAM, ELDREDGE (2004-02-01). "Evolutionary Relationships, Cospeciation, and Host Switching in Avian Malaria Parasites".Systematic Biology.53(1): 111–119.CiteSeerX10.1.1.496.1628.doi:10.1080/10635150490264987.ISSN1063-5157.PMID14965906.
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  10. ^Engel, Joshua (8 April 2015)."Birds get malaria, too".Field Museum of Natural History.Archivedfrom the original on 25 February 2022.Retrieved25 February2022.
  11. ^Bensch, Staffan; Hellgren, Olof; Pérez-Tris, Javier (2009-09-01). "MalAvi: a public database of malaria parasites and related haemosporidians in avian hosts based on mitochondrial cytochrome b lineages".Molecular Ecology Resources.9(5): 1353–1358.doi:10.1111/j.1755-0998.2009.02692.x.ISSN1755-0998.PMID21564906.S2CID1447832.
  12. ^Martinsen, Ellen S.; Perkins, Susan L.; Schall, Jos J. (2008-04-01). "A three-genome phylogeny of malaria parasites (Plasmodium and closely related genera): Evolution of life-history traits and host switches".Molecular Phylogenetics and Evolution.47(1): 261–273.Bibcode:2008MolPE..47..261M.doi:10.1016/j.ympev.2007.11.012.PMID18248741.
  13. ^Hellgren, Olof; Atkinson, Carter T.; Bensch, Staffan; Albayrak, Tamer; Dimitrov, Dimitar; Ewen, John G.; Kim, Kyeong Soon; Lima, Marcos R.; Martin, Lynn (2015-08-01). "Global phylogeography of the avian malaria pathogen Plasmodium relictum based on MSP1 allelic diversity".Ecography.38(8): 842–850.Bibcode:2015Ecogr..38..842H.doi:10.1111/ecog.01158.ISSN1600-0587.S2CID85890180.
  14. ^BENSCH, STAFFAN; HELLGREN, OLOF; PÉREZ-TRIS, JAVIER (2009-08-12). "MalAvi: a public database of malaria parasites and related haemosporidians in avian hosts based on mitochondrial cytochrome b lineages".Molecular Ecology Resources.9(5).Wiley:1353–1358.doi:10.1111/j.1755-0998.2009.02692.x.ISSN1755-098X.PMID21564906.S2CID1447832.
  15. ^Pigeault, Romain; Vézilier, Julien; Cornet, Stéphane; Zélé, Flore; Nicot, Antoine; Perret, Philippe; Gandon, Sylvain; Rivero, Ana (2015-08-19)."Avian malaria: a new lease of life for an old experimental model to study the evolutionary ecology ofPlasmodium".Philosophical Transactions of the Royal Society B: Biological Sciences.370(1675). TheRoyal Society:20140300.doi:10.1098/rstb.2014.0300.ISSN0962-8436.PMC4528498.PMID26150666.S2CID7896992.
  16. ^"How to Protect Hawaii's Rarest Birds From Avian Malaria".Audubon.2015-11-16.Archivedfrom the original on 2020-02-04.Retrieved2020-02-04.
  17. ^"The Nobel Prize in Physiology or Medicine 1907".NobelPrize.org.Retrieved2023-10-19.
  18. ^Prevention, CDC-Centers for Disease Control and (2017-03-28)."CDC - Malaria - About Malaria - History - Ross and the Discovery that Mosquitoes Transmit Malaria Parasites".cdc.gov.Retrieved2023-10-19.
  19. ^Sinden, RE (2007)."Malaria, mosquitoes and the legacy of Ronald Ross".Bulletin of the World Health Organization.85(11): 894–896.doi:10.2471/blt.04.020735(inactive 1 November 2024).PMC2636258.PMID18038083.{{cite journal}}:CS1 maint: DOI inactive as of November 2024 (link)
  20. ^"Avian malaria | Bird Disease, Causes & Prevention | Britannica".britannica.Retrieved2023-10-26.
  21. ^abcUSDI and USGS 2005.
  22. ^Warner 1968; Van Riper 1991; USDI and USGS 2005.
  23. ^GaramszegI, László Z (2011). "Climate change increases the risk of malaria in birds".Global Change Biology.17(5): 1751–1759.Bibcode:2011GCBio..17.1751G.doi:10.1111/j.1365-2486.2010.02346.x.S2CID84073382.
  24. ^Booth, Mark (2018-03-28).Climate Change and the Neglected Tropical Diseases.Advances in Parasitology. Vol. 100.Elsevier.pp. 39–126.doi:10.1016/bs.apar.2018.02.001.ISBN9780128151693.ISSN0065-308X.PMC7103135.PMID29753342.
  25. ^Specter, Michael (15 July 2016)."How the DNA Revolution Is Changing Us".National Geographic Magazine.Archived fromthe originalon 22 May 2020.Retrieved21 April2019.

Further reading

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