Psittacine beak and feather disease: Difference between revisions

Browse history interactively ← Previous edit Next edit →Content deleted Content addedVisual WikitextInline

Revision as of 08:08, 28 September 2020 editEvolution and evolvability (talk \| contribs)Extended confirmed users24,410 edits + references from v:WikiJournal_of_Science/Beak_and_feather_disease_virus:_biology_and_resultant_disease under CC BY license (doi:10.15347/wjs/2020.007)Tag: 2017 wikitext editor ← Previous edit		Revision as of 08:10, 28 September 2020 edit undoEvolution and evolvability (talk \| contribs)Extended confirmed users24,410 edits + Host range and transmission from v:WikiJournal_of_Science/Beak_and_feather_disease_virus:_biology_and_resultant_disease under CC BY license (doi:10.15347/wjs/2020.007)Tag: 2017 wikitext editor Next edit →
Line 46:		Line 46:

	== Host range and transmission ==		== Host range and transmission ==
	BFDV infection was thought to be restricted to within ], but evidence of host switching among distantly-related Australian avian species was recently demonstrated in the ] (''Merops ornatus''), ] (''Ninox strenua'') and ]. A large number of other non-psittacine birds are likely susceptible to sporadic spill-over infection, and there is unpublished evidence of BFDV-associated feather disease in the ] (''Daceolo novaeguineae''), ], ] and raptors including the ] (''Aquila audax''), ] (''Haliaetus leucogaster''), ] (''Falco peregrinus'') and ] (''Haliastur sphenurus''). However, the actual mechanism of this host-switch event in raptors and other species is not well understood. Presumably, it occurs in raptors and other birds following predation and/or opportunistic feeding upon the tissues or excretions of BFDV-affected parrots and cockatoos. '']'' mites have recently been shown to concentrate BFDV within their faeces which raises the possibility of ectoparasites such as ] acting as ] and vectors of transmission particularly to insectivorous bird species such as the rainbow bee-eater. Interestingly, while interseasonal nest hollow sharing may promote the circulation of novel BFDV genotypes in psittacine populations, species such as raptors, which retain nest hollows over many seasons, may not have sufficient intraspecific transmission frequencies to permit permanent host switching.		BFDV infection was thought to be restricted to within ], but evidence of host switching among distantly-related Australian avian species was recently demonstrated in the ] (''Merops ornatus''),<ref name="Sarker et al., 2015b"/> ] (''Ninox strenua'')<ref name="Sarker et al., 2016a"/> and ].<ref name="Circella et al., 2014"/> A large number of other non-psittacine birds are likely susceptible to sporadic spill-over infection,<ref name="Amery-Gale et al., 2017"/> and there is unpublished evidence of BFDV-associated feather disease in the ] (''Daceolo novaeguineae''), ], ] and raptors including the ] (''Aquila audax''), ] (''Haliaetus leucogaster''), ] (''Falco peregrinus'') and ] (''Haliastur sphenurus'').<ref name="Raidal and Peters, 2018"/> However, the actual mechanism of this host-switch event in raptors and other species is not well understood. Presumably, it occurs in raptors and other birds following predation and/or opportunistic feeding upon the tissues or excretions of BFDV-affected parrots and cockatoos. '']'' mites have recently been shown to concentrate BFDV within their faeces<ref name="Portas et al., 2017"/> which raises the possibility of ectoparasites such as ] acting as ] and vectors of transmission particularly to insectivorous bird species such as the rainbow bee-eater. Interestingly, while interseasonal nest hollow sharing may promote the circulation of novel BFDV genotypes in psittacine populations, species such as raptors, which retain nest hollows over many seasons, may not have sufficient intraspecific transmission frequencies to permit permanent host switching.<ref name="Raidal and Peters, 2018"/>

	Beak and feather disease virus is the dominant viral pathogen of Psittaciformes in Australasia, where it has been present for at least 10 million years, and Australia has been identified as the most likely origin of the virus. The richness of psittacine avifauna in this region has produced a mixture of potential hosts for the pathogens, resulting in competing forces of virus co-evolution, spill-over infection and virus host-switches within parrots, cockatoos and lorikeets. Recent evidence has shown that all threatened and endangered Australian psittacine bird species can be infected by BFDV genotypes from any other closely- or distantly-related host reservoir species. Currently, more than 78 psittacine bird species globally have been reported to be infected by BFDV, including at least 38 of the 50 Australian native parrot species both in captivity and the wild, and over 25 non-psittacine bird species.		Beak and feather disease virus is the dominant viral pathogen of Psittaciformes in Australasia, where it has been present for at least 10 million years,<ref name="Raidal and Peters, 2018"/> and Australia has been identified as the most likely origin of the virus.<ref name="Harkins et al., 2014"/> The richness of psittacine avifauna in this region has produced a mixture of potential hosts for the pathogens, resulting in competing forces of virus co-evolution, spill-over infection and virus host-switches within parrots, cockatoos and lorikeets. Recent evidence has shown that all threatened and endangered Australian psittacine bird species can be infected by BFDV genotypes from any other closely- or distantly-related host reservoir species.<ref name="Raidal et al., 2015"/><ref name="Sarker et al., 2015a"/> Currently, more than 78 psittacine bird species globally have been reported to be infected by BFDV, including at least 38 of the 50 Australian native parrot species both in captivity and the wild, and over 25 non-psittacine bird species.<ref name="Amery-Gale et al., 2017"/><ref name="Das et al., 2016a"/><ref name="Department of the Environment and Heritage, 2005"/><ref name="Eastwood et al., 2014"/><ref name="Fogell et al., 2016"/><ref name="Raidal and Peters, 2018"/><ref name="Sarker et al., 2014c"/><ref name="Sarker et al., 2016a"/><ref name="Sarker et al., 2015b"/><ref name="Sarker et al., 2014d"/>

⚫	Transmission is thought to include both horizontal and vertical modalities. In wild bird populations, transmission of infection most likely occurs within nest hollows by oral or intracloacal ingestion of the virus possibly sourced from feather dust, crop secretions, or faeces. Although there has been debate in the literature concerning the role of vertical transmission of avian circovirus, BFDV is suspected to be transmitted vertically because viral DNA can be found in embryos from infected hens. However, this could simply be the result of non-replicative transfer of viral DNA into the yolk of embryonated eggs. Further investigations are required in this regard.

		⚫	Transmission is thought to include both horizontal and vertical modalities. In wild bird populations, transmission of infection most likely occurs within nest hollows by oral or intracloacal ingestion of the virus possibly sourced from feather dust, crop secretions, or faeces.<ref name="Ritchie et al., 1991"/><ref name="Wylie and Pass, 1987"/> Although there has been debate in the literature concerning the role of vertical transmission of avian circovirus, BFDV is suspected to be transmitted vertically because viral DNA can be found in embryos from infected hens.<ref name="Rahaus et al., 2008"/> However, this could simply be the result of non-replicative transfer of viral DNA into the yolk of embryonated eggs. Further investigations are required in this regard.
	== Infection paths ==		== Infection paths ==
	PBFD is usually acquired by nestlings from their parents (]) or from other members of the flock (]). The immature immune system of young birds makes them susceptible to the PBFDV. The virus may be transferred in ] secretions, in fresh or dried ], and in feather and skin particles.		PBFD is usually acquired by nestlings from their parents (]) or from other members of the flock (]). The immature immune system of young birds makes them susceptible to the PBFDV. The virus may be transferred in ] secretions, in fresh or dried ], and in feather and skin particles.

Revision as of 08:10, 28 September 2020

Beak and feather disease virus
Virus classification
(unranked):	Virus
Realm:	Monodnaviria
Kingdom:	Shotokuvirae
Phylum:	Cressdnaviricota
Class:	Arfiviricetes
Order:	Cirlivirales
Family:	Circoviridae
Genus:	Circovirus
Species:	Beak and feather disease virus

Psittacine beak and feather disease (PBFD) is a viral disease affecting all Old World and New World parrots. The causative virus–beak and feather disease virus (BFDV)—belongs to the taxonomic genus Circovirus, family Circoviridae. It attacks the feather follicles and the beak and claw matrices of the bird, causing progressive feather, claw and beak malformation and necrosis. In later stages of the disease, feather shaft constriction occurs, hampering development until eventually all feather growth stops. It occurs in an acutely fatal form and a chronic form.

Cracking and peeling of the outer layers of the claws and beak make tissues vulnerable to secondary infection. Because the virus also affects the thymus and Bursa of Fabricius, slowing lymphocyte production, immunosuppression occurs and the bird becomes more vulnerable to secondary infections. Beak fractures and necrosis of the hard palate can prevent the bird from eating.

History

The ornithologist Edwin Ashby observed a flock of completely featherless red-rumped parrots (Psephotus haematonotus) in the Adelaide Hills, South Australia, in 1888. The species then disappeared from the area for several years.

The condition is more prevalent in widely occurring Australian species such as the sulphur-crested cockatoo, little corella and galah.

The first case of chronic PBFD was reported in a Control and Therapy article in 1972 for the University of Sydney by Ross Perry, in which he described it as "beak rot in a cockatoo". Dr. Perry subsequently studied the disease and wrote extensively about its clinical features in a range of psittacine birds in a long article in which he named the disease "psittacine beak and feather disease syndrome" (PBFDS). This soon became known as psittacine beak and feather disease (PBFD).

Beak and feather disease virus

PBFD is caused by the Beak and feather disease virus (BFDV), a circular or icosahedral, 14–16 nm diameter, single-stranded circular DNA, non-enveloped virus with a genome size of between 1992 and 2018 nucleotides. It encodes seven open reading frames—three in the virion strand and four in the complementary strand. The open reading frames have some homology to porcine circovirus (family Circoviridae), subterranean clover stunt virus and faba bean necrotic yellows virus (both family Nanoviridae).

History

It was first isolated and characterized by researchers Dr. David Pass of Murdoch University in Perth and Dr. Ross Perry from Sydney, with later work at the University of Georgia in the United States, the University of Sydney and Murdoch University in Australia, and the University of Cape Town, among other centres. The virus was originally designated PCV (psittacine circovirus), but has since been renamed beak and feather disease virus. This is due in part, to the research confirming that this virus is the cause of the disease, and in part to avoid confusion with Porcine circovirus, also called PCV.

Detection

A variety of tests for the presence of BFDV are available: standard polymerase chain reaction (PCR), quantitative PCR (qPCR) which can detect the virus in extremely small quantities, whole-genome sequencing, histology, immunohistochemical tests, and quantitative haemagglutination assays.

Structure

Transmission electron micrograph of BFDV infected cell on the right demonstrating how the nucleus (N) is relatively sparse, with large crystalline arrays of mature virus particles preferentially forming intracytoplasmic inclusions (V) shown at higher magnification on the left

Structural characterisation of two BFDV capsid virions. X-ray crystal structures allow modelling of the two particles to 1.9 Å (10 nm-immature virions, left), and 2.5 Å (60 nm-mature virions, right). The smaller particle is composed of 10 capsid molecules arranged as two interlocking discs, with each disc containing five capsid molecules. The larger VLP consists of 12 pentamers arranged with T=1 icosahedral symmetry.

The beak and feather disease virus (BFDV) is currently considered a member of the family Circoviridae. Like other circoviruses, BFDV possesses a small, circular single-stranded DNA (ssDNA) genome (approximately 2.0 kb in length) that is encapsidated into a non-enveloped, spherical icosahedral virion. In order to replicate its genome, BFDV needs to invade the nucleus to access the transcriptional machinery of the host cell. The replication of BFDV is known to occur in numerous tissues, including skin, liver, gastrointestinal tract, and bursa of Fabricius; while the capsid antigen of BFDV is found in the spleen, thymus, thyroid, parathyroid and bone marrow. However, the distinction between viral entry and replication in a host cell remains unclear in the absence of confirmation in suitable cell culture. Viral attachment and entry into host cells may not necessarily lead to viral replication, and consequently not all cells containing viral particles may contribute to the disease progression. However, it is thought that the BFDV encodes proteins that actively transport the viral genome into the nucleus, as well as factors that direct the precursor DNA exit to the cytoplasm, where it causes large globular intracytoplasmic paracrystalline arrays (Figure 1).

The BFDV genome is bi-directionally transcribed and encodes at least two major proteins: a replication initiation protein (rep) expressed from the virion strand and a capsid protein (cap) expressed from the complementary strand. A recent study conducted by Sarker et al. used a combination of X-ray crystallography, cryo-electron microscopy and atomic force microscopy to investigate the functionality of cap and its interaction with a range of host and viral proteins. They confirmed that the cap protein forms virus-like particles (VLPs) of ~17 nm (mature form) and a smaller assembly of ~10 nm (immature form) (Figure 2). Furthermore, this study demonstrated that assembly of these two VLPs is regulated by single-stranded DNA (ssDNA), and that they provide a structural basis of capsid assembly around single-stranded DNA.

Host range and transmission

BFDV infection was thought to be restricted to within Psittaciformes, but evidence of host switching among distantly-related Australian avian species was recently demonstrated in the rainbow bee-eater (Merops ornatus), powerful owl (Ninox strenua) and finches. A large number of other non-psittacine birds are likely susceptible to sporadic spill-over infection, and there is unpublished evidence of BFDV-associated feather disease in the laughing kookaburra (Daceolo novaeguineae), columbids, corvids and raptors including the wedge-tailed eagle (Aquila audax), white-breasted sea eagle (Haliaetus leucogaster), peregrine falcon (Falco peregrinus) and whistling kite (Haliastur sphenurus). However, the actual mechanism of this host-switch event in raptors and other species is not well understood. Presumably, it occurs in raptors and other birds following predation and/or opportunistic feeding upon the tissues or excretions of BFDV-affected parrots and cockatoos. Knemidokoptes mites have recently been shown to concentrate BFDV within their faeces which raises the possibility of ectoparasites such as hippoboscid flies acting as fomites and vectors of transmission particularly to insectivorous bird species such as the rainbow bee-eater. Interestingly, while interseasonal nest hollow sharing may promote the circulation of novel BFDV genotypes in psittacine populations, species such as raptors, which retain nest hollows over many seasons, may not have sufficient intraspecific transmission frequencies to permit permanent host switching.

Beak and feather disease virus is the dominant viral pathogen of Psittaciformes in Australasia, where it has been present for at least 10 million years, and Australia has been identified as the most likely origin of the virus. The richness of psittacine avifauna in this region has produced a mixture of potential hosts for the pathogens, resulting in competing forces of virus co-evolution, spill-over infection and virus host-switches within parrots, cockatoos and lorikeets. Recent evidence has shown that all threatened and endangered Australian psittacine bird species can be infected by BFDV genotypes from any other closely- or distantly-related host reservoir species. Currently, more than 78 psittacine bird species globally have been reported to be infected by BFDV, including at least 38 of the 50 Australian native parrot species both in captivity and the wild, and over 25 non-psittacine bird species.

Transmission is thought to include both horizontal and vertical modalities. In wild bird populations, transmission of infection most likely occurs within nest hollows by oral or intracloacal ingestion of the virus possibly sourced from feather dust, crop secretions, or faeces. Although there has been debate in the literature concerning the role of vertical transmission of avian circovirus, BFDV is suspected to be transmitted vertically because viral DNA can be found in embryos from infected hens. However, this could simply be the result of non-replicative transfer of viral DNA into the yolk of embryonated eggs. Further investigations are required in this regard.

Infection paths

PBFD is usually acquired by nestlings from their parents (vertical transmission) or from other members of the flock (horizontal transmission). The immature immune system of young birds makes them susceptible to the PBFDV. The virus may be transferred in crop secretions, in fresh or dried feces, and in feather and skin particles.

Adult birds coming into contact with the virus usually (but not always) develop resistance to it, but the virus is retained in their body and, in most cases, is excreted in feces and feather debris for the rest of their lives.

Signs and symptoms

The acute form of the disease is manifested by lethargy, loss of appetite, vomiting and diarrhea. Due to the severe immune system suppression, multiple secondary infections develop, causing death within two to four weeks. Typical confirmation of the acute form of the disease is by necropsy, because it progresses too quickly for the normal signs such as feather loss and beak deformity to appear.

The chronic form occurs if the bird's immune system manages to mount a reaction to the virus and any secondary infections. The characteristic feather symptoms need time to develop, as they only appear during the first moult after infection. In those species having powder down, signs may be visible immediately, as powder down feathers are continually replenished.

Threat

PBFD has the potential to become a major threat to all species of wild parrots and to modern aviculture, due to international legal and illegal bird trade. Cases of PBFD have now been reported in at least 78 psittacine species. At least 38 of 50 Australian native species are affected by PBFD, both captive and in the wild. In 2004, PBFD was listed as a key threatening process by the Australian Commonwealth Government for the survival of five endangered species, including one of the few remaining species of migratory parrots, the orange-bellied parrot, of which only an estimated 3 mating pairs remained in 2017.

Treatment

There is currently no specific treatment for the virus. A vaccine is available, but only experimentally. It has not been released to the public due to the risk it poses to already exposed birds.

Therapeutic intervention is limited to treating secondary infections. The individual bird can sometimes recover or have an acceptable quality of life if the symptoms are mild/progress slowly.

The management of the disease lies thus mostly in prevention. Every new bird that enters a pen with other birds should be quarantined first and be tested for BFDV. Birds which are known carriers should not be introduced into new pens, especially not if those contain young birds.

References

Pyne, M. Psittacine Beak and Feather Disease. Currumbin Wildlife Sanctuary, Gold Coast. National Wildlife Rehabilitation Conference 2005.
Ashby, E. (1921). Notes on Psephotus hematonotus, the Red-rumped Grass Parrakeet. The Avicultural Magazine Third Series, Vol. XII. pg 131.
Borthwick, D. Threat Abatement Plan for Psittacine Beak and Feather Disease Affecting Endangered Psittacine Species. Department of the Environment and Heritage, Commonwealth of Australia. 2005.
^ Perry, R.A. (197?) Proc 55, PGCVSc, University of Sydney, pp. ?-?
Bassami MR, Berryman D, Wilcox GE, Raidal SR (1998). "Psittacine beak and feather disease virus nucleotide sequence analysis and its relationship to porcine circovirus, plant circoviruses, and chicken anaemia virus". Virology. 249 (2): 453–9. doi:10.1006/viro.1998.9324. PMID 9791035.
^ Fogell, Deborah J.; Martin, Rowan O.; Groombridge, Jim J. (2016-05-05). "Beak and feather disease virus in wild and captive parrots: an analysis of geographic and taxonomic distribution and methodological trends". Archives of Virology. 161 (8): 2059–74. doi:10.1007/s00705-016-2871-2. ISSN 0304-8608. PMC 4947100. PMID 27151279.
Sarker, S.; Terrón, M.C.; Khandokar, Y.; Aragão, D.; Hardy, J.M.; Radjainia, M.; Jiménez-Zaragoza, M.; de Pablo, P.J.; Coulibaly, F.; Luque, D.; Raidal, S.R.; Forwood, J.K. (2016). "Structural insights into the assembly and regulation of distinct viral capsid complexes". Nature Communications. 7: 13014. doi:10.1038/ncomms13014.
^ Sarker, S.; Moylan, K.G.; Ghorashi, S.A.; Forwood, J.K.; Peters, A.; Raidal, S.R. (2015). "Evidence of a deep viral host switch event with beak and feather disease virus infection in rainbow bee-eaters (Merops ornatus)". Scientific Reports. 5: 14511. doi:10.1038/srep14511.
^ Sarker, S.; Lloyd, C.; Forwood, J.; Raidal, S.R. (2016). "Forensic genetic evidence of beak and feather disease virus infection in a Powerful Owl, Ninox strenua". Emu. 116 (1): 71–74. doi:10.1071/MU15063.
Circella, E.; Legretto, M.; Pugliese, N.; Caroli, A.; Bozzo, G.; Accogli, G.; Lavazza, A.; Camarda, A. (2014). "Psittacine Beak and Feather Disease–like Illness in Gouldian Finches (Chloebia gouldiae)". Avian Diseases. 58 (3): 482–487. doi:10.1637/10745-121113case.1.
^ Amery-Gale, J.; Marenda, M.S.; Owens, J.; Eden, P.A.; Browning, G.F.; Devlin, J.M. (2017). "A high prevalence of beak and feather disease virus in non-psittacine Australian birds". Journal of Medical Microbiology. 66: 1005–1013. doi:10.1099/jmm.0.000516.
^ Raidal, S.R.; Peters, A. (2018). "Psittacine beak and feather disease: ecology and implications for conservation". Emu. 118 (1): 80–93. doi:10.1080/01584197.2017.1387029.
Portas, T.; Jackson, B.; Das, S.; Shamsi, S.; Raidal, S. R. (2017). "Beak and feather disease virus carriage by Knemidocoptes pilae in a sulphur‐crested cockatoo (Cacatua galerita)". Australian Veterinary Journal. 95 (12): 486–489. doi:10.1111/avj.12649.
Harkins, G.W.; Martin, D.P.; Christoffels, A.; Varsani, A. (2014). "Towards inferring the global movement of beak and feather disease virus". Virology. 450–451: 24–33. doi:10.1016/j.virol.2013.11.033.
Raidal, S.R.; Sarker, S.; Peters, A. (2015). "Review of psittacine beak and feather disease and its effect on Australian endangered species". Australian Veterinary Journal. 93 (12): 466–470. doi:10.1111/avj.12388.
Sarker, S.; Forwood, J.K.; Ghorashi, S.A.; Peters, A.; Raidal, S.R. (2015). "Beak and feather disease virus genotypes in Australian parrots reveal flexible host-switching". Australian Veterinary Journal. 93 (12): 471–475. doi:10.1111/avj.12389.
Das, S.; Sarker, S.; Ghorashi, S.A.; Forwood, J.K.; Raidal, S.R. (2016). "A comparison of PCR assays for beak and feather disease virus and high resolution melt (HRM) curve analysis of replicase associated protein and capsid genes". Journal of Virological Methods. 237: 47–57. doi:10.1016/j.jviromet.2016.08.015.
Department of the Environment and Heritage (2005). Threat Abatement Plan for Psittacine Beak and Feather Disease affecting endangered psittacine species.Canberra, ACT 2601 (PDF) (Report). Department of the Environment and Heritage, Commonwealth of Australia.
Eastwood, J.R.; Berg, M.L.; Ribot, R.F.; Raidal, S.R.; Buchanan, K.L.; Walder, K.R.; Bennett, A.T. (2014). "Phylogenetic analysis of beak and feather disease virus across a host ring-species complex". Proceedings of the National Academy of Sciences. 111 (39): 14153–14158. doi:10.1073/pnas.1403255111.
Fogell, D.J.; Martin, R.O.; Groombridge, J.J. (2016). "Beak and feather disease virus in wild and captive parrots: an analysis of geographic and taxonomic distribution and methodological trends". Archives of Virology. 161 (8): 2059–2074. doi:10.1007/s00705-016-2871-2.
Sarker, S.; Ghorashi, S.A.; Forwood, J.K.; Bent, J.S.; Peters, A.; Raidal, S.R. (2014). "Phylogeny of beak and feather disease virus in cockatoos demonstrates host generalism and multiple-variant infections within Psittaciformes". Virology. 460–461: 72–82. doi:10.1016/j.virol.2014.04.021.
Sarker, S.; Ghorashi, S.A.; Forwood, J.K.; Raidal, S.R. (2014). "Rapid genotyping of beak and feather disease virus using high-resolution DNA melt curve analysis". Journal of Virological Methods. 208: 47–55. doi:10.1016/j.jviromet.2014.07.031.
Ritchie, B.W.; Niagro, F.D.; Latimer, K.S.; Steffens, W.L.; Pesti, D.; Ancona, J.; Lukert, P.D. (1991). "Routes and prevalence of shedding of psittacine beak and feather disease virus". American Journal Veterinary Research. 52 (11): 1804–1809.
Wylie, S.L.; Pass, D.A. (1987). "Experimental reproduction of psittacine beak and feather disease french moult". Avian Pathology. 16 (2): 269–281. doi:10.1080/03079458708436374.
Rahaus, M.; Desloges, N.; Probst, S.; Loebbert, B.; Lantermann, W.; Wolff, M.H. (2008). "Detection of beak and feather disease virus DNA in embryonated eggs of psittacine birds". Veterinarni Medicina. 53 (1): 53–58. doi:10.17221/1932-VETMED.
Beak and feather disease virus (BFDV) (micro-organism). Global Invasive Species Database. ISSG. IUCN.
"Beak and Feather disease".

Cite error: A list-defined reference named "Ashby" is not used in the content (see the help page).
Cite error: A list-defined reference named "Chae et al., 2020" is not used in the content (see the help page).
Cite error: A list-defined reference named "Das et al., 2016b" is not used in the content (see the help page).
Cite error: A list-defined reference named "dept of env" is not used in the content (see the help page).
Cite error: A list-defined reference named "Khalesi et al., 2005" is not used in the content (see the help page).
Cite error: A list-defined reference named "Latimer et al., 1990" is not used in the content (see the help page).
Cite error: A list-defined reference named "Morinha et al., 2020" is not used in the content (see the help page).
Cite error: A list-defined reference named "Ogawa et al., 2005" is not used in the content (see the help page).
Cite error: A list-defined reference named "Pass & Perry, 1984" is not used in the content (see the help page).
Cite error: A list-defined reference named "Raidal and Cross, 1995" is not used in the content (see the help page).
Cite error: A list-defined reference named "Raidal and Cross, 1994" is not used in the content (see the help page).
Cite error: A list-defined reference named "Raidal et al., 1993a" is not used in the content (see the help page).
Cite error: A list-defined reference named "Raidal et al., 1993b" is not used in the content (see the help page).
Cite error: A list-defined reference named "Ramis et al., 1994" is not used in the content (see the help page).
Cite error: A list-defined reference named "Ritchie, 1995" is not used in the content (see the help page).
Cite error: A list-defined reference named "Ritchie et al., 1990" is not used in the content (see the help page).
Cite error: A list-defined reference named "Ritchie et al., 1989" is not used in the content (see the help page).
Cite error: A list-defined reference named "Sarker et al., 2014a" is not used in the content (see the help page).
Cite error: A list-defined reference named "Sarker et al., 2014b" is not used in the content (see the help page).
Cite error: A list-defined reference named "Shearer et al., 2008" is not used in the content (see the help page).
Cite error: A list-defined reference named "Shearer et al., 2009" is not used in the content (see the help page).
Cite error: A list-defined reference named "Varsani et al., 2011" is not used in the content (see the help page).

Cite error: A list-defined reference named "Ypelaar et al., 1999" is not used in the content (see the help page).

Misplaced Pages