Abstract
Passeriformes populations have experienced a marked decline in number during the last decades. Several infectious agents have been described as key factors for this population’s decrease, as they can cause mortal diseases like the recently reported Suttonella ornithocola. S. ornithocola is a bacterium from the Cardiobacteriaceae family that has been linked to several outbreaks. This systematic review aims to collect all the scientific information available about S. ornithocola to better understand its epidemiology and pathogenesis and to assess the potential hazard that it can pose to garden songbirds. Although it has been considered a respiratory pathogen, S. ornithocola has been isolated from several organs, suggesting a systemic pathogenesis. However, it has also been described as a normal taxon from the microbiota of some bird species. Therefore, further studies in healthy birds are necessary to establish if S. ornithocola is a primary pathogen or an opportunistic bacterium in songbirds.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
No datasets were generated or analysed during the current study.
Availability of data and materials
Not applicable.
References
Alba C, Sansano-Maestre J, Cid Vázquez MD, Martínez-Herrero MDC, Garijo-Toledo MM, Azami-Conesa I, Moraleda Fernández V, Gómez-Muñoz MT Rodríguez JM (2022) Captive breeding and Trichomonas gallinae alter the oral microbiome of Bonelli’s eagle chicks. Microb Ecol 1–11. https://doi.org/10.1007/s00248-022-02002-y
Bates JM, Fidino M, Nowak-Boyd L, Strausberger BM, Schmidt KA, Whelan CJ (2023) Climate change affects bird nesting phenology: comparing contemporary field and historical museum nesting records. J Anim Ecol 92(2):263–272. https://doi.org/10.1111/1365-2656.13683
Ben-Asher HW, Yerushalmi R, Wachtel C, Barbiro-Michaely E, Sompolinsky D, Gerber D (2017) Draft genome sequence of the Suttonella ornithocola bacterium. Genome Announc 5(7):10–1128. https://doi.org/10.1128/genomea.01592-16
Burns F, Eaton MA, Burfield IJ, Klvaňová A, Šilarová E, Staneva A, Gregory RD (2021) Abundance decline in the avifauna of the European Union reveals cross-continental similarities in biodiversity change. Ecol Evol 11(23):16647–16660. https://doi.org/10.1002/ece3.8282
Çakır Bayram L, Abay S, Satıcıoğlu İB, Güvenç T, Ekebaş G, Aydın F (2021) The ocular pyogranulomatous lesion in a Gentoo penguin (Pygoscelis papua) from the Antarctic Peninsula: evaluation of microbiological and histopathological analysis outcomes. Vet Res Commun 45:143–158. https://doi.org/10.1007/s11259-021-09796-1
Černá K (2023) Interspecific and intraspecific variation in gastrointestinal microbiota composition of parrots and its association with incidence of selected disorders. Diploma thesis, Charles University, Prague. http://hdl.handle.net/20.500.11956/185867
Colvile KM, Lawson B, Pocknell AM, Dagleish MP, John SK, Cunningham AA (2012) Chlamydiosis in British songbirds. Vet Rec 171(7):177–182. https://doi.org/10.1136/vr.100506
D’Agnese E, McLaughlin RJ, Lea MA, Soto E, Smith WA, Bowman JP (2023) Comparative microbial community analysis of fur seals and aquaculture salmon gut microbiomes in Tasmania. In Oceans 4(2):200–219. MDPI. https://doi.org/10.3390/oceans4020014
Dominguez-Sanchez C, Alvarez-Martinez R, Gendron D, Acevedo-Whitehouse K (2022) Core respiratory microbiome of the blue whale, Balaenoptera musculus. bioRxiv 2022–12. https://doi.org/10.1101/2022.12.29.522252
Fischer L, Peters M, Merbach S, Eydner M, Kuczka A, Lambertz J, Kummerfeld M, Kahnt K, Weiss A, Petersen H (2021) Increased mortality in wild tits in North Rhine-Westphalia (Germany) in 2020 with a special focus on Suttonella ornithocola and other infectious pathogens. Eur J Wildl Res 67(3):56. https://doi.org/10.1007/s10344-021-01500-7
Foster G, Malnick H, Lawson PA, Kirkwood J, MacGregor SK, Collins MD (2005) Suttonella ornithocola sp. nov., from birds of the tit families, and emended description of the genus Suttonella. Int J Syst Evol Microbiol 55(6):2269–2272. https://doi.org/10.1099/ijs.0.63681-0
Gomes AVS, Quinteiro-Filho WM, Ribeiro A, Ferraz-de-Paula V, Pinheiro ML, Baskeville E, Akamine AT, Astolfi-Ferreira CS, Ferreira AJP, Palermo-Neto J (2014) Overcrowding stress decreases macrophage activity and increases Salmonella Enteritidis invasion in broiler chickens. Avian Pathol 43(1):82–90. https://doi.org/10.1080/03079457.2013.874006
Gregory RD, Skorpilova J, Vorisek P, Butler S (2019) An analysis of trends, uncertainty and species selection shows contrasting trends of widespread forest and farmland birds in Europe. Ecol Ind 103:676–687. https://doi.org/10.1016/j.ecolind.2019.04.064
Hanmer HJ, Cunningham AA, John SK, Magregor SK, Robinson RA, Seilern-Moy K, Siriwardena GM, Lawson B (2022) Habitat-use influences severe disease-mediated population declines in two of the most common garden bird species in Great Britain. Sci Rep 12(1):15055. https://doi.org/10.1038/s41598-022-18880-8
Herder EA, Spence AR, Tingley MW, Hird SM (2021) Elevation correlates with significant changes in relative abundance in hummingbird fecal microbiota, but composition changes little. Front Ecol Evol 8:597756. https://doi.org/10.3389/fevo.2020.597756
Huso MM, Dalthorp D (2014) Accounting for unsearched areas in estimating wind turbine-caused fatality. J Wildl Manag 78(2):347–358. https://doi.org/10.1002/jwmg.663
Janda WM (2013) Update on the HACEK group of fastidious gram-negative bacilli. Part II Clin Microbiol Newslett 35(12):95–101. https://doi.org/10.1016/j.clinmicnews.2013.05.004
Kinney ME, Ericsson AC, Franklin CL, Whiting RE, Pearce JW (2017) Ocular findings and select ophthalmic diagnostic tests in captive American white pelicans (Pelecanus erythrorhynchos). J Zoo Wildlife Med: Offic Public Am Assoc Zoo Vet 48(3):675. https://doi.org/10.1638/2F2016-0256.1
Kirkwood JK, Macgregor SK, Malnick H, Foster G (2006) Unusual mortality incidents in tit species (family Paridae) associated with the novel bacterium. Vet Rec 158:203–205. https://doi.org/10.1136/vr.158.6.203
Kissel LN, Bankowski MJ, Koyamatsu TL, Nagai RY, Seifried SE, Crow GL (2011) Aerobic microorganisms identified over a fourteen-month period from the upper respiratory tract of captive Hawaiian monk seals (Monachus schauinslandi). Aquatic Mammals 37(3). https://doi.org/10.1578/AM.37.3.2011.377
Koleček J, Adamík P, Reif J (2020) Shifts in migration phenology under climate change: temperature vs. abundance effects in birds. Climatic Change 159(2):177–194. https://doi.org/10.1007/s10584-020-02668-8
Lawson B, Malnick H, Pennycott TW, Macgregor SK, John SK, Duncan G, Hughes L, Chantrey J, Cunningham AA (2011) Acute necrotising pneumonitis associated with Suttonella ornithocola infection in tits (Paridae). Vet J 188(1):96–100. https://doi.org/10.1016/j.tvjl.2010.03.010
Lawson B, Robinson RA, Colvile KM, Peck KM, Chantrey J, Pennycott TW, Simpson VR, Toms MP, Cunningham AA (2012) The emergence and spread of finch trichomonosis in the British Isles. Philos Transact Royal Soc b: Biol Sci 367(1604):2852–2863. https://doi.org/10.1098/rstb.2012.0130
Leclaire S, Pineaux M, Blanchard P, White J, Hatch SA (2022) Microbiota composition and diversity of multiple body sites vary according to reproductive performance in a seabird. Mol Ecol. https://doi.org/10.1111/mec.16398
Leitzen E, Peters M, Merbach S, Wohlsein P, Baumgärtner W (2022) Suttonella ornithocola detected within lesions of tit birds (Paridae) from epidemic death episodes in Germany, 2018–2020. Front Vet Sci 9. https://doi.org/10.3389/fvets.2022.977570
Madoroba E, Magwedere K, Chaora NS, Matle I, Muchadeyi F, Mathole MA, Pierneef R (2021) Microbial communities of meat and meat products: an exploratory analysis of the product quality and safety at selected enterprises in South Africa. Microorganisms 9(3):507. https://doi.org/10.3390/microorganisms9030507
Merbach S, Peters M, Kilwinski J, Reckling D (2019) Suttonella ornithocola-associated mortality in tits in Germany. Berliner und Münchener Tierärztliche Wochenschrift. 132(9/10):459–463. ISSN: 0005–9366
Milliere L, Loïez C, Patoz P, Charlet A, Duployez C, Wallet F (2022) Apyretic pulmonary oedema revealing Cardiobacterium hominis endocarditis: case report and review of literature. Idcases 29:e01506. https://doi.org/10.1016/j.idcr.2022.e01506
Montecillo JAV (2023) Phylogenomics and comparative genomic analyses support the creation of the novel family Ignatzschineriaceae fam. nov. comprising the genera Ignatzschineria and Wohlfahrtiimonas within the order Cardiobacteriales. Res Microbiol 174(1–2):103988. https://doi.org/10.1016/j.resmic.2022.103988
Oettel J, Lapin K (2021) Linking forest management and biodiversity indicators to strengthen sustainable forest management in Europe. Ecol Ind 122:107275. https://doi.org/10.1016/j.ecolind.2020.107275
Peniche G, Fernandez JRR, Durrant C, John SK, Macgregor SK, Cunningham AA, Lawson B (2017) Nested PCR for Suttonella ornithocola reveals widespread infection in British Paridae species. Eur J Wildl Res 63:1–9. https://doi.org/10.1007/s10344-017-1105-6
Pennycott TW (2016) Diseases of wild birds of the orders Passeriformes and Columbiformes-a review of conditions reported from the United Kingdom and an analysis of results from wild bird disease surveillance in Scotland 1994–2013. PhD Dissertation, The University of Edinburgh. http://hdl.handle.net/1842/23001
Soares-Castro P, Araújo-Rodrigues H, Godoy-Vitorino F, Ferreira M, Covelo P, López A, Vingada J, Eira C, Santos PM (2019) Microbiota fingerprints within the oral cavity of cetaceans as indicators for population biomonitoring. Sci Rep 9(1):13679. https://doi.org/10.1038/s41598-019-50139-7
Taylor MJ, Mannan RW, U’Ren JM, Garber NP, Gallery RE, Arnold AE (2019) Age-related variation in the oral microbiome of urban Cooper’s hawks (Accipiter cooperii). BMC Microbiol 19(1):1–10. https://doi.org/10.1186/s12866-019-1413-y
Wobeser G, Wobeser AG (1992) Carcass disappearance and estimation of mortality in a simulated die-off of small birds. J Wildl Dis 28(4):548–554. https://doi.org/10.7589/0090-3558-28.4.548
Zanolari P, Dürr S, Jores J, Steiner A, Kuhnert P (2021) Ovine footrot: a review of current knowledge. Vet J 271:105647. https://doi.org/10.1016/j.tvjl.2021.105647
Author information
Authors and Affiliations
Contributions
Conceptualization: B.M.M. and F.E.; Literature research and data analysis: B.M.M.; Writing – original draft: B.M.M.; Writing – review and editing: F.E.
Corresponding author
Ethics declarations
Ethical approval
Not applicable.
Competing interests
The authors declare no competing interests.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Martín-Maldonado, B., Esperón, F. Can Suttonella ornithocola entail a potential hazard to songbirds? A systematic review. Eur J Wildl Res 70, 29 (2024). https://doi.org/10.1007/s10344-024-01785-4
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s10344-024-01785-4