Avipoxvirus

Pictures

Picture	Title	Caption	Copyright
Title Mature pox virus particle Caption Thin section electron microscopy showing a mature pox virus particle, with a centrally located biconcave core, two lateral bodies and the outer coat. Copyright Natàlia Majó Masferror	Mature pox virus particle	Thin section electron microscopy showing a mature pox virus particle, with a centrally located biconcave core, two lateral bodies and the outer coat.	Natàlia Majó Masferror
Title Histopathology Caption Histopathology of a pox lesion, showing epithelial hypertrophy and inclusion bodies. Copyright U.S. Geological Survey/Pacific Island Ecosystems Research Center, Hawaii	Histopathology	Histopathology of a pox lesion, showing epithelial hypertrophy and inclusion bodies.	U.S. Geological Survey/Pacific Island Ecosystems Research Center, Hawaii
Title Pox virus infected CAM Caption Pox virus infected CAM. Note diffuse thickening of the membrane. Copyright Laboratorios Hipra, S.A.	Pox virus infected CAM	Pox virus infected CAM. Note diffuse thickening of the membrane.	Laboratorios Hipra, S.A.
Title Cutaneous pox virus symptoms. Caption Cutaneous form of pox virus infection. Variously sized papules or nodules are observed in the comb of this animal. Copyright Natàlia Majó Masferror	Cutaneous pox virus symptoms.	Cutaneous form of pox virus infection. Variously sized papules or nodules are observed in the comb of this animal.	Natàlia Majó Masferror
Title Histology Caption Histologic section of poxvirus-infected CAM. Epithelial hyperplasia and large, eosinophilic intracytoplasmic inclusion bodies (Bollinger bodies) within epithelial cells are observed. Copyright Natàlia Majó Masferror	Histology	Histologic section of poxvirus-infected CAM. Epithelial hyperplasia and large, eosinophilic intracytoplasmic inclusion bodies (Bollinger bodies) within epithelial cells are observed.	Natàlia Majó Masferror
Title Diptheric form symptoms Caption Diphteric form of pox virus infection. Yellowish pseudomembranes are observed in the lumen of the trachea.|Diphteric form of pox virus infection. Yellowish pseudomembranes are observed in the lumen of the trachea. Yellowish pseudomembranes are observed in the lumen of the trachea. Copyright Laboratorios Hipra, S.A.	Diptheric form symptoms	Diphteric form of pox virus infection. Yellowish pseudomembranes are observed in the lumen of the trachea.|Diphteric form of pox virus infection. Yellowish pseudomembranes are observed in the lumen of the trachea. Yellowish pseudomembranes are observed in the lumen of the trachea.	Laboratorios Hipra, S.A.
Title Symptoms Caption Nodule in a feathered area of a pigeon caused by pox virus infection. Copyright Natàlia Majó Masferror	Symptoms	Nodule in a feathered area of a pigeon caused by pox virus infection.	Natàlia Majó Masferror
Title Histology Caption Histologic section of poxvirus-infected skin. Epithelial hyperplasia and large, eosinophilic intracytoplasmic inclusion bodies (Bollinger bodies) within epithelial cells are observed. Copyright Natàlia Majó Masferror	Histology	Histologic section of poxvirus-infected skin. Epithelial hyperplasia and large, eosinophilic intracytoplasmic inclusion bodies (Bollinger bodies) within epithelial cells are observed.	Natàlia Majó Masferror
Title Symptoms Caption Characteristic pox lesions on the feet of an immature apapane, Hawaii Island. Copyright U.S. Geological Survey/Pacific Island Ecosystems Research Center, Hawaii	Symptoms	Characteristic pox lesions on the feet of an immature apapane, Hawaii Island.	U.S. Geological Survey/Pacific Island Ecosystems Research Center, Hawaii
Title Symptoms Caption Cutaneous pox lesions on the bill and eyelid of nestling Laysan Albatross, Midway Atoll National Wildlife Refuge. Copyright U.S. Fish and Wildlife Service	Symptoms	Cutaneous pox lesions on the bill and eyelid of nestling Laysan Albatross, Midway Atoll National Wildlife Refuge.	U.S. Fish and Wildlife Service

Identity

Preferred Scientific Name

• Avipoxvirus International Committee on Taxonomy of Viruses (ICTV), 2009

Other Scientific Names

• Poxvirus avium

Summary of Invasiveness

Avian poxviruses (Avipoxvirus spp.) are large DNA viruses that cause disease in over 200 species of domestic and wild birds (van Riper and Forrester, 2008). Avian pox occurs worldwide and is typically an endemic, mild, and self-limiting disease among wild birds. Outbreaks, however, often occur in captive situations, such as zoos and game farms, where bird densities are high.  Epizootics among endemic birds on remote islands (Hawaiian Islands, since circa 1902 [van Riper et al., 2004]; Galapagos Archipelago, since circa 1971 [Vargas, 1987]; Canary Islands, since 2000 [Smits et al., 2005]; Falkland Islands, since circa 1962 [Munro, 2006]) are characterized by high morbidity and mortality and indicate the invasive nature of avian pox. Invasiveness of avian poxvirus is due in part to its ability to withstand extreme environmental conditions and be transmitted by ingestion of contaminated food, water and aerosols, biting arthropods, or by any means that brings virus in direct contact with living epithelial cells (van Riper and Forrester, 2007). Avipoxvirus is listed as an invasive microorganism by the IUCN - Invasive Species Specialists Group (ISSG, 2008).

Taxonomic Tree

• Domain: Virus
•     Group: "ssDNA viruses"
•         Group: "DNA viruses"
•             Family: Poxviridae
•                 Subfamily: Chordopoxvirinae
•                     Genus: Avipoxvirus

Diseases Table

Distribution

Avian poxviruses occur worldwide except in the Arctic and some remote island locations (van Riper and Forrester, 2007; Shearn-Bochsler et al., 2008).  There are fewer published reports from Africa and South America but this probably reflects limited research activity and not a natural distribution.  In North America they appear to be more prevalent in the warmer and moister regions of the United States (van Riper and Forrester, 2007).  Where it has been reported on remote oceanic islands, like the Hawaiian Islands, Galapagos Islands and Canary Islands, avian poxvirus behaves as an invasive species, spreading rapidly among susceptible species and causing higher mortality.

Distribution Table

The distribution in this summary table is based on all the information available. When several references are cited, they may give conflicting information on the status. Further details may be available for individual references in the Distribution Table Details section which can be selected by going to Generate Report.

History of Introduction and Spread

In the Hawaiian Islands, there are no clear accounts of when avian pox first arrived. Fowlpox was likely introduced during the 1800s with the importation of domestic fowl (Riper et al., 2002).  Spread of avian pox must have accelerated after the introduction of the Southern House Mosquito, Culex quinquefasciatus, around 1827 (LaPointe, 2007). Naturalist bird collectors had observed pox-like lesions on native forest birds and speculated on its impact throughout the 1890s (Henshaw, 1902). Fowlpox was first officially diagnosed on domestic chickens in 1901 and, a year later, avian pox was diagnosed in an endemic forest bird, the akepa (Loxops coccineus) (Riper et al., 2002). Presumed, and confirmed, avian pox epizootics have been reported in the Hawaiian Crow (Corvus hawaiiensis) (Jenkins et al., 1989) on Hawaii Island and in endemic Hawaiian honeycreepers (Drepanidinae) (Riper et al., 2002; Atkinson et al., 2005; Aruch et al., 2007) throughout the islands. Avipoxvirus was identified from a Red-tailed Tropicbird (Phaethon rubricauda) on Midway Atoll in the northwest Hawaiian Islands in 1963 (Locke et al., 1965) and epizootics of avian pox among nesting seabirds have regularly occurred on Midway Atoll since then (Sileo et al., 1990). A recent molecular analysis of contemporary pox lesions from native birds and historical lesions from museum specimens revealed that at least one variant (Variant 2) of contemporary Hawaiian forest bird Avipoxvirus was present in 1900 (Jarvi et al., 2008). The two variants of Hawaiian forest bird Avipoxvirus are genetically distinct from fowlpox and more similar to canarypox suggesting separate introductions of the two apparent species (Jarvi et al., 2008).

In the Galapagos Islands, avian pox viruses may have been introduced with domestic chickens before the twentieth century as there are unpublished accounts of pox-like lesions as early as 1905 (Wikelski et al., 2004). Based on histological examination, lesions from Darwin’s Finches (Geospiza spp.) were identified as avian pox in 1971 (Vargas, 1987).  Pox-like lesions were reported from Galapagos mockingbirds (Nesomimus parvulus) on Isla Santa Cruz in 1979 (Vargas, 1987) and epizootics of presumed avian pox commonly occur in yellow warblers (Dendroica petechia), Galapagos doves (Zenaida galapagoensis), Galapagos mockingbirds, and Galapagos finches (Geospiza spp.) on the inhabited islands and islets of Santa Cruz and Isabella (Thiel et al., 2005).  Avian pox was also suspected during an epizootic among Galapagos mockingbirds on the islands of Genovesa, Champion, and Gardner during the El Niño-Southern Oscillation (ENSO) event of 1982-1983 (Curry and Grant, 1989; Grant et al., 2000). The Black Salt Marsh Mosquito, Ochlerotatus taeniorhynchus [Aedestaeniorhynchus], is native to the Galapagos Islands and may serve as a vector of Avipoxvirus (Bataille et al., 2009).  However, in 1985, Culex quinquefasciatus was first collected on Isla Santa Cruz (Whiteman et al., 2005) and the establishment of this avid, bird feeding mosquito on inhabited islands may have accelerated the spread and prevalence of avian pox.  Recent molecular analysis of Avipoxvirus from chickens and endemic passerines in the Galapagos revealed fowlpox among chickens and two canarypox-like strains (Gal1 and Gal 2) among endemic passerines (Thiel et al., 2005). The original virus affecting endemic passerines may have come from domestic songbirds or migrating wild passerines.

Avian pox was first observed on White-tailed Laurel Pigeons (Columba junoniae) on La Palma in the Canary Islands in 2000 (Medina et al., 2004). In 2002, an epizootic of avian pox in Short-toed Larks (Calandrella rufescens) and Berthelot’s Pipits (Anthus berthelotti) was reported from the islands of Fuerteventura and Lanzarote.  Poultry fleas may have driven the spread of Avipoxvirus during the epizootic (Smits et al., 2005).  Avian pox has since been detected on 5 of the 9 islands that make up the Canaries and Porto Santos in the Maderian archipelago (Illera et al., 2008). Eleven mosquito species are known from the Canary Islands including the Northern House Mosquito, Culex pipiens, which was introduced to these islands prior to the mid-1800s (Baez and Fernandez, 1980).

In the Falkland Islands, avian pox was first reported from domestic chickens and the Black-browed Albatross (Thalassarche melanophris [Diomedeamelanophris]) in 1987; however, suspected avian pox infections had been reported in albatross colonies as early as 1962.  An avian pox outbreak in the Falklands in 2006 killed approximately 200 Gentoo Penguins (Pygoscelis papua) (Munro, 2006). Scavenging birds such as gulls, vultures, and skuas may have spread the virus from domestic sites to breeding colonies.  Researchers may also have spread Avipoxvirus from one rookery to another.  In 2004, avian poxvirus was detected in a nestling Southern Giant Petrel (Macronectes giganteus) from Anvers Island, Antarctica (Shearn-Bochsler et al., 2008). In the case of southern giant petrels, adult birds likely brought the virus to the nesting colony, but the origin and initial route of infection in the adult birds is unknown.

Introductions

Risk of Introduction

Avipoxvirus appears to be present throughout most of the continental regions of the world and absent, for the most part, from the most remote polar regions and oceanic islands (Riper and Forrester, 2007).  The main route of introduction to these remote areas is likely to be infected hosts transported as part of the commercial poultry, game and pet bird trade (van Riper et al., 2002; Foster, 2009).  Migratory wild birds may also spread the virus from mainland areas to less remote islands (Thiel et al., 2005). Due to the environmental stability of the virus, however, the reuse and resale of contaminated cages or equipment may also serve as a route of entry. Virus might also arrive with mosquito vectors that are common stowaways in aircraft cabins and cargo holds (Lounibos, 2002).

Once established in an archipelago, virus may be spread interisland by migrating or dispersing wild birds, arthropod vectors (windblown or as stowaways on aircraft or ships), or even on the soles of contaminated boots after people have visited farms, poultry houses, rearing facilities, or seabird rookeries.  Avian researchers and recreational birders may inadvertently spread the virus if they are not diligent in the disinfection of all footwear, clothing, tripods, mist nets, traps, and banding equipment when working between or visiting diseased and disease-free areas (Munro, 2006).

Pathogen Characteristics

Avian poxvirus is a large, enveloped DNA virus ranging from 260 to 309 kilobase pairs long with a G+C content of 35% and molecular weight of 185±5 x 10⁶ daltons.  All avian poxviruses show identical morphology. The brick-shape virions measure approximately 330x280x200 nanometres and are covered with surface knobs (Tripathy, 1993). While poxviruses are typically resistant to ether, some avian poxvirus species/strains are sensitive to ether and chloroform. Avian poxvirus can withstand temperature as high as 50°C for 30 minutes and 60ºC for 8 minutes (Tripathy, 1993). The virus can withstand desiccation for several months or years.  The viruses develop in the cytoplasm of avian epithelial cells forming characteristic inclusions known as Bollinger bodies which consist, by weight, of 50% extractable lipids (Tripathy, 1993). Species differentiation in the past has been based on host specificity and antigenic similarities (Kirmse, 1967) but recent molecular work has begun to differentiate avian poxvirus species and strains by gene sequencing (Tripathy and Reed, 2003).

Host Animals

Climate

Notes on Natural Enemies

There are no natural enemies of Avipoxvirus.

Pathway Causes

Pathway Vectors

Vectors and Intermediate Hosts

Economic Impact

In chickens, cutaneous fowlpox seldom results in economically significant mortality; however, the diphtheritic form of fowlpox can cause up to 60% mortality in unvaccinated chickens.  Cutaneous fowlpox can cause a transient drop in layer egg production, up to 15%, and reduces growth rate in young birds (Beckman, 2007).  On a flock basis, outbreaks of fowlpox generally last 6-10 weeks resulting in significant economic loss in egg production.  For domestic turkeys, the reduced weight gain in market birds has a larger impact (Cunningham, 1978).  Septicaemic canarypox can have a great impact on individual commercial canary breeders due to the high incidence and mortality rates associated with this form of the disease (Ritchie, 1995).

Environmental Impact

Impact on biodiversity

Although avian pox is typically an endemic, mild, and self-limiting disease among wild birds, epizootics among endemic birds on remote islands  such as the Hawaiian Islands, (van Riper et al., 2004), Galapagos Archipelago (Vargas, 1987), Canary Islands (Smits et al., 2005) and Falkland Islands (Munro, 2006) are characterized by high morbidity and mortality.

Threatened Species

Risk and Impact Factors

• Proved invasive outside its native range
• Has a broad native range
• Abundant in its native range
• Highly adaptable to different environments
• Fast growing
• Has high reproductive potential
• Has propagules that can remain viable for more than one year
• Reproduces asexually
• Has high genetic variability

• Host damage
• Negatively impacts agriculture
• Negatively impacts animal health
• Negatively impacts livelihoods
• Reduced native biodiversity
• Threat to/ loss of endangered species
• Threat to/ loss of native species
• Negatively impacts animal/plant collections

• Interaction with other invasive species
• Pathogenic

• Highly likely to be transported internationally accidentally
• Highly likely to be transported internationally illegally
• Difficult to identify/detect as a commodity contaminant
• Difficult/costly to control

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Links to Websites

Organizations

UK: Falklands Conservation, 1 Princes Avenue, London N3 2DA, http://www.falklandsconservation.com/

USA: USDA-APHIS-NVSL: UDSA Animal and Plant Health Inspection Service, National Veterinary Services Laboratory, PO Box 844, Ames, IA 50010, http://www.aphis.usda.gov/animal_health/lab_info_services/

USA: USGS-NWHC - National Wildlife Health Center, 6006 Schroeder Road Madison, Wisconsin 53711, http://www.nwhc.usgs.gov/

USA: USGS-PIERC: Pacific Island Ecosystems Research Center, Kilauea Field Station, PO Box 44, Hawaii National Park Hawaii, http://biology.usgs.gov/pierc/

Galapagos Islands: Charles Darwin Research Station (CDRS), run by the Charles Darwin Foundaton, Puerto Ayora, Isla Santa Cruz, Galapagos, http://www.darwinfoundation.org/english/pages/index.php

Contributors

21/07/10 Original text by:

Dennis LaPointe, US Geological Survey, Hawaii, USA

Distribution Maps