New insights into avian malaria infections in New Zealand seabirds.

Plasmodium Birds Disease LINN1 Petrel Procellariiformes

Journal

Parasitology research
ISSN: 1432-1955
Titre abrégé: Parasitol Res
Pays: Germany
ID NLM: 8703571

Informations de publication

Date de publication:
16 Apr 2024
Historique:
received: 26 01 2024
accepted: 11 04 2024
medline: 16 4 2024
pubmed: 16 4 2024
entrez: 16 4 2024
Statut: epublish

Résumé

The past few years have been marked by a drastic increase in pathogen spillover events. However, the extent and taxonomic range at which these events take place remain as crucial unanswered questions in many host-pathogen systems. Here, we take advantage of opportunistically sampled bird carcasses from the South Island of New Zealand, with the aim of identifying Plasmodium spp. infections in native and endemic New Zealand seabird species. In total, six samples from five bird species were positive for avian malaria, including four of which were successfully sequenced and identified as Plasmodium matutinum LINN1 lineage. These results provide new Plasmodium infection records in seabirds, including the first documented case in Procellariiformes in New Zealand, highlighting the potential disease risk to these species.

Identifiants

pubmed: 38625416
doi: 10.1007/s00436-024-08210-4
pii: 10.1007/s00436-024-08210-4
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

184

Subventions

Organisme : Cawthron Institute
ID : CAWX2207

Informations de copyright

© 2024. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.

Références

Agüero M, Monne I, Sánchez A, Zecchin B, Fusaro A, Ruano MJ, ..., Orejas JJ (2023) Highly pathogenic avian influenza A(H5N1) virus infection in farmed minks, Spain, October 2022. Euro Surveill 28(3):2300001. https://doi.org/10.2807/1560-7917.ES.2023.28.3.2300001
Alley M, Hale K, Cash W, Ha H, Howe L (2010) Concurrent avian malaria and avipox virus infection in translocated South Island saddlebacks (Philesturnus carunculatus carunculatus). N Z Vet J 58:218–223
pubmed: 20676161 doi: 10.1080/00480169.2010.68868
Alley MR, Hunter SA, Webster T (2019) An outbreak of avian malaria in yellow-eyed penguins, Megadyptes antipodes. Kokako 26:21–22
Atkinson CT, Samuel MD (2010) Avian malaria Plasmodium relictum in native Hawaiian forest birds: epizootiology and demographic impacts on ‘Apapane Himatione sanguinea. J Avian Biol 41:357–366
doi: 10.1111/j.1600-048X.2009.04915.x
Banks-Leite C, Pardini R, Tambosi LR, Pearse WD, Bueno AA, Bruscagin RT, Condez TH, Dixo M, Igari AT, Martensen AC, Metzger JP (2014) Using ecological thresholds to evaluate the costs and benefits of set-asides in a biodiversity hotspot. Science 345:1041–1045
pubmed: 25170150 doi: 10.1126/science.1255768
Bensch S, Hellgren O, Pérez-Tris J (2009) MalAvi: A public database of malaria parasites and related heamosporidians in avian hosts based on mitochondrial cytochrome b lineage. Mol Ecol Resour 9:1353–1358
pubmed: 21564906 doi: 10.1111/j.1755-0998.2009.02692.x
Castro I, Howe L, Tompkins DM, Barraclough RK, Slaney D (2011) Presence and seasonal prevalence of Plasmodium spp. in a rare endemic New Zealand passerine (tieke or Saddleback, Philesturnus carunculatus). J Wildl Dis 47:860–867
pubmed: 22102656 doi: 10.7589/0090-3558-47.4.860
Cloutier A, Mills J, Yarrall J, Baker A (2011) Plasmodium infections of red-billed gulls (Larus scopulinus) show associations with host condition but not reproductive performance. J R Soc N Z 41:261–277
doi: 10.1080/03036758.2011.559662
Cunningham A (1996) Disease risks of wildlife translocations. Conserv Biol 10:349–353
doi: 10.1046/j.1523-1739.1996.10020349.x
Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 30:772
doi: 10.1038/nmeth.2109
Daszak P, Cunningham A, Hyatt A (2000) Emerging infectious diseases of wildlife - threats to biodiversity and human health. Science 287:443–449
pubmed: 10642539 doi: 10.1126/science.287.5452.443
Ewen JG, Bensch S, Blackburn TM, Bonneaud C, Brown R, Cassey P, Clarke RH, Pérez-Tris J (2012) Establishment of exotic parasites: the origins and characteristics of an avian malaria community in an isolated island avifauna. Ecol Lett 15:1112–1119
pubmed: 22788956 doi: 10.1111/j.1461-0248.2012.01833.x
Filion A, Deschamps L, Niebuhr CN, Poulin R (2022) Anthropogenic landscape alteration promotes higher disease risk in wild New Zealand avian communities. PLoS ONE 17(3):e0265568
pubmed: 35333899 pmcid: 8956180 doi: 10.1371/journal.pone.0265568
Filion A, Webster T, Poulin R, Godfrey SS (2023) Interannual patterns of avian diseases in wild New Zealand avifauna near conservation areas. Austral Ecol 48:1413–1425
doi: 10.1111/aec.13400
Guidon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704
doi: 10.1080/10635150390235520
Gulliver E, Hunter S, Howe L, Castillo-Alcala F (2022) The pathology of fatal avian malaria due to Plasmodium elongatum (GRW6) and Plasmodium matutinum (LINN1) infection in New Zealand kiwi (Apteryx spp.). Animals 12:3376
pubmed: 36496898 pmcid: 9740581 doi: 10.3390/ani12233376
Heard MJ, Smith KF, Ripp KJ, Berger M, Chen J, Dittmeier J, Goter M, Mcgarvey ST, Ryan E (2013) The threat of disease increases as species move toward extinction. Conserv Biol 27:1378–1388
pmcid: 4398030 doi: 10.1111/cobi.12143
Hellgren O, Waldenström J, Bensch S (2004) A new PCR assay for simultaneous studies of Leucocytozoon, Plasmodium, and Haemoproteus from avian blood. J Parasitol 90:797–802
pubmed: 15357072 doi: 10.1645/GE-184R1
Hof C, Araujo MB, Jetz W, Rahlbek C (2011) Additive threats from pathogens, climate and land-use change for global amphibian diversity. Nature 480:516–519
pubmed: 22089134 doi: 10.1038/nature10650
Howe L, Castro IC, Schoener ER, Hunter S, Barraclough RK, Alley MR (2012) Malaria parasites (Plamodium spp.) infecting introduced, native and endemic New Zealand birds. Parasitol Res 110:913–923
pubmed: 21842389 doi: 10.1007/s00436-011-2577-z
Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17:754–755
pubmed: 11524383 doi: 10.1093/bioinformatics/17.8.754
Hunter SA (2015) Avian malaria caused by Plasmodium elongatum in a Fiordland crested penguin. Kokako 22:21–22
Krammer F, Schultz-Cherry S (2023) We need to keep an eye on avian influenza. Nat Rev Immunol 23:267–268. https://doi.org/10.1038/s41577-023-00868-8
doi: 10.1038/s41577-023-00868-8 pubmed: 36944755 pmcid: 10028763
Lapointe DA, Atkinson CT, Samuel MD (2012) Ecology and conservation of avian malaria. Ann N Y Acad Sci 1249:211–226
pubmed: 22320256 doi: 10.1111/j.1749-6632.2011.06431.x
Lymbery AJ, Morine M, Kanani HG, Beatty SJ, Morgan DL (2014) Co-invaders: the effects of alien parasites on native hosts. Int J Parasitol 3:171–177
Meister SL, Richard OK, Hoby S, Gurtner C, Basso WU (2021) Fatal avian malaria in captive Atlantic puffins (Fratercula arctica) in Switzerland. Int J Parasitol: Parasit Wildl 14:97–106
Miller MA, Pfeiffer W, Schwartz T (2010) Creating the CIPRES Science Gateway for inference of large phylogenetic trees Gateway Computing Environments Workshop (GCE). LA, USA, New Orleans, pp 1–8
Niebuhr CN, Blasco-Costa I (2016) Improving detection of avian malaria from host blood: a step towards a standardised protocol for diagnostics. Parasitol Res 115:3905–3911
pubmed: 27249965 doi: 10.1007/s00436-016-5157-4
Niebuhr CN, Poulin R, Tompkins DM (2016) Is avian malaria playing a role in native bird decline in New Zealand? Testing the hypotheses along an elevational gradient. PLoS ONE 11:e0165918
pubmed: 27802326 pmcid: 5089714 doi: 10.1371/journal.pone.0165918
Rambaut A, Drummond AJ, Xie D, Baele G, Suchard MA (2018) Posterior summarization in Bayesian phylogenetics using tracer 1.7. Syst Biol 67:901–904
pubmed: 29718447 pmcid: 6101584 doi: 10.1093/sysbio/syy032
Robertson HA, Baird KA, Elliott GP, Hitchmough RA, McArthur NJ, Makan TD, Miskelly CM, O’Donnell CJF, Sagar PM, Scofield RP, Taylor GA, Michel P (2021) Conservation status of birds in Aotearoa New Zealand, 2021. New Zealand Threat Classification Series 36. Wellington, New Zealand
Roche B, Dobson AP, Guégan JF, Rohani P (2012) Linking community and disease ecology: the impact of biodiversity on pathogen transmission. Philos Trans R Soc Lond B Biol Sci 367:2807–2813
pubmed: 22966136 pmcid: 3427561 doi: 10.1098/rstb.2011.0364
Schoener ER, Banda M, Howe L, Castro IC, Alley MR (2014) Avian malaria in New Zealand. NZ Vet J 62:189–198
doi: 10.1080/00480169.2013.871195
Schoener ER, Tompkins DM, Parker KA, Howe L, Castro I (2020) Presence and diversity of mixed avian Plasmodium spp. infections in introduced birds whose distribution overlapped with threatened New Zealand endemic birds. N Z Vet J 68:101–106
pubmed: 31645214 doi: 10.1080/00480169.2019.1680326
Sijbranda DC, Campbell J, Gartrell BD, Howe L (2016) Avian malaria in introduced, native and endemic New Zealand bird species in a mixed ecosystem. N Z J Ecol 40:72–79
doi: 10.20417/nzjecol.40.8
Smith KF, Sax DE, Lafferty KD (2006) Evidence for the role of infectious disease in species extinction and endangerment. Conserv Biol 20:1349–1357
pubmed: 17002752 doi: 10.1111/j.1523-1739.2006.00524.x
Spottiswoode N, Bartlett SL, Conley KJ, Seimon TA, Griffin DO, Sykes JM (2020) Analysis of Plasmodium lineages identified in captive penguins (Sphenisciformes spp.), eiders (Somateria spp.), and Inca terns (Larosterna inca) in a North American zoological collection. J Zoo Wildl Med 51:140
pubmed: 32212557 doi: 10.1638/2019-0078
Suzán G, García-Peña GE, Castro-Arellano I, Rico O, Rubio AV et al (2015) Metacommunity and phylogenetic structure determine wildlife and zoonotic infectious disease patterns in time and space. Eco Evol 5:865–873
doi: 10.1002/ece3.1404
Svensson-Coelho M, Silva GT, Santos SS, Miranda LS, Araújo-Silva LE, Ricklefs RE, Miyaki CY, Maldonado-Coelho M (2016) Lower detection probability of avian plasmodium in blood compared to other tissues. J Parasitol 02:559–561
doi: 10.1645/16-8
Tabak MA, Piaggio AJ, Miller RS, Sweitzer RA, Ernest HB (2017) Anthropogenic factors predict movement of an invasive species. Ecosphere 8:e01844
doi: 10.1002/ecs2.1844
Tompkins DM, Gleeson DM (2006) Relationship between avian malaria distribution and an exotic invasive mosquito in New Zealand. J R Soc N Z 36:51–62
doi: 10.1080/03014223.2006.9517799
Tompkins DM, Poulin R (2006) Biological invasions in New-Zealand p. 67–82. Parasites and biological invasions. Springer-Verlag, Berlin Heidelberg, p 461
Tompkins DM, Carver S, Jones ME, Krkošek M, Skerratt LF (2015) Emerging infectious diseases of wildlife: a critical perspective. Trends Parasitol 31:149–159
pubmed: 25709109 doi: 10.1016/j.pt.2015.01.007
Valente L, Etienne RS, Garcia-R JC (2019) Deep macroevolutionary impact of humans on New Zealand’s unique avifauna. Curr Biol 29:2563–2569
pubmed: 31386837 doi: 10.1016/j.cub.2019.06.058
Valkiūnas G, Ilgunas M, Bukauskaite D, Palinauskas V, Bernotiene R, Iezhova TA (2017) Molecular characterization and distribution of Plasmodium matutinum, a common avian malaria parasite. Parasitology 144:1726–1735
pubmed: 28931453 doi: 10.1017/S0031182017000737
Van Riper III C, Van Riper SG, Goff ML, Laird M (1986) The epizootiology and ecological significance of malaria in Hawaiian land birds. Ecol Monogr 56:327–344
doi: 10.2307/1942550
Veltman CJ, Nee S, Crawley MJ (1996) Correlates of introduction success in exotic New Zealand birds. Am Nat 147:542–557
doi: 10.1086/285865
Wilkinson DA, Marshall JC, French NP, Hayman DTS (2018) Habitat fragmentation, biodiversity loss and the risk of novel infectious disease emergence. J R Soc Interface 15:20180403
pubmed: 30518565 pmcid: 6303791 doi: 10.1098/rsif.2018.0403
Wood MJ, Cosgrove CL, Wilkin TA, Knowles SCL, Day KP, Sheldon BC (2007) Within-population variation in prevalence and lineage distribution of avian malaria in blue tits, Cyanistes caeruleus. Mol Ecol 16:3263–3273
pubmed: 17651202 doi: 10.1111/j.1365-294X.2007.03362.x

Auteurs

Jerusha Bennett (J)

Department of Zoology, University of Otago, 340 Great King St, Dunedin, 9016, New Zealand.

Chris N Niebuhr (CN)

Manaaki Whenua - Landcare Research, PO Box 69040, Lincoln, 7640, New Zealand.

Clément Lagrue (C)

New Zealand Department of Conservation, 265 Princes St, Dunedin, 9016, New Zealand.

Karen L Middlemiss (KL)

New Zealand Department of Conservation, Munro Building, 186 Bridge Street, Nelson, 7010, New Zealand.

Trudi Webster (T)

Yellow-Eyed Penguin Trust, 265 Princes St, Dunedin, 9016, New Zealand.

Antoine Filion (A)

Department of Integrative Biology, 501 Life Sciences West, Oklahoma State University, Stillwater, OK, 74078, USA. afilion90@gmail.com.

Classifications MeSH