Abstract
The haematophagous mite Ornithonyssus sylviarum may cause important economic losses in commercial poultry farms whilst also potentially affecting the health of farm workers. The dynamics of this ectoparasite has been linked to several factors, including wild birds, fomites, farm workers, management of hen houses, and host traits. Along two consecutive years, we carried out systematic sampling at three laying hen farms located in Santa Fe province, Argentina, with the aim of identifying factors that may influence O. sylviarum prevalence and intensity. We found that the density of feathers around the hen vent area and the presence of Menoponidae lice were negatively associated with mite abundance. We also found that the density of hens in the cages was negatively associated with mite prevalence, suggesting a possible dilution effect, whereas prior reports found a positive association with hen density. In addition, summer was the season with minimum mite prevalences and intensities, contrary to previous studies in northern farms where warm weather appeared to prompt an increase in mite populations. Another factor associated with mite intensity was age, but this effect varied depending on the season, which hints that the association between hen’s age and mites is complex. Basic epidemiological knowledge on O. sylviarum in poultry farms from South America may aid in a more efficient and integrative approach to its control.
This is a preview of subscription content, access via your institution.








Availability of data and material
Detailed data will be made available upon request.
Code availability
Not applicable.
References
Aramburú R, Calvo S, Alzugaray M, Cicchino A (2003) Ectoparasitic load of monk parakeet (Myopsitta monachus, Psittacidae) nestlings. Ornitologia Neotropical 14:415–418
Arce SI, Manzoli DE, Saravia-Pietropaolo MJ et al (2018) The tropical fowl mite, Ornithonyssus bursa (Acari: Macronyssidae): environmental and host factors associated with its occurrence in Argentine passerine communities. Parasitol Res 117:3257–3267. https://doi.org/10.1007/s00436-018-6025-1
Arce SI, Monje LD, Antoniazzi LR et al (2020) Mesostigmatid mites (Acari: Mesostigmata) at the domestic-wildlife interface: poultry and passerine birds of central Argentina. Vet Parasitol 284:109203. https://doi.org/10.1016/j.vetpar.2020.109203
Arrabal JP, Manzoli DE, Antoniazzi LR et al (2012) Prevalencia del ácaro Ornithonyssus bursa Berlese, 1888 (Mesostigmata: Macronyssidae) en un ensamble de aves (Passeriformes) de bosques del centro de la Provincia de Santa Fe, Argentina. Rev Ibero-Latinoam Parasitol 71:172–178
Arthur FH, Axtell RC (1982) Northern fowl mite population development on laying hens caged at three colony sizes. Poult Sci 62:424–427
Axtell RC, Arends JJ (1990) Ecology and management of arthropod pests of poultry. Annu Rev Entomol 35:101–126
Blersch R, Bonnell TR, Barrett L, Henzi SP (2021) Seasonal effects in gastrointestinal parasite prevalence, richness and intensity in vervet monkeys living in a semi-arid environment. J Zool 314:163–173. https://doi.org/10.1111/jzo.12877
Bommarito C, Wahl M, Thieltges DW et al (2022) Biotic and abiotic drivers affect parasite richness, prevalence and abundance in Mytilus galloprovincialis along the Northern Adriatic Sea. Parasitology:1–9. https://doi.org/10.1017/S0031182021001438
Burg JG, Collison CH, Mastro AM (1988) Comparative analysis of precipitating antibodies in White Rock and Fayoumi hens injected with bovine serum albumin or crude mite extract with resulting effects on northern fowl mite, Ornithonyssus sylviarum (Acari: Macronyssidae) population densities. Poult Sci 67:1015–1019. https://doi.org/10.3382/ps.0671015
Burnham KP, Anderson DR (2004) Multimodel inference: understanding AIC and BIC in model selection. Sociol Methods Res 33:261–304. https://doi.org/10.1177/0049124104268644
Castignani H (2011) Zonas Agroeconómicas Homogéneas Santa Fe. Estudios socioeconómicos de la sustentabilidad de los sistemas de producción y recursos naturales. Instituto Nacional de Tecnología Agropecuaria, Buenos Aires, p 61
Chaisiri K, McGarry JW, Morand S, Makepeace BL (2015) Symbiosis in an overlooked microcosm: a systematic review of the bacterial flora of mites. Parasitology 142:1152–1162. https://doi.org/10.1017/S0031182015000530
Chang Y, Wang XJ, Feng JH et al (2018) Real-time variations in body temperature of laying hens with increasing ambient temperature at different relative humidity levels. Poult Sci 97:3119–3125. https://doi.org/10.3382/ps/pey184
Chen BL, Haith KL, Mullens BA (2011) Beak condition drives abundance and grooming-mediated competitive asymmetry in a poultry ectoparasite community. Parasitology 138:748–757. https://doi.org/10.1017/S0031182011000229
Chen BL, Mullens BA (2008) Temperature and humidity effects on off-host survival of the northern fowl mite (Acari : Macronyssidae) and the chicken body louse (Phthiraptera: Menoponidae). Vet Entomol 101:637–646
Christensen RHB (2019) Ordinal–regression models for ordinal data. R package version 2019.12–10. Accessed 31 Jul 2020
Crutchfield CM, Hixson H (1943) Food habits of several species of poultry lice with special reference to blood consumption. Fla Entomol 26:63–66. https://doi.org/10.1093/besa/16.4.185b
Crystal MM (1985) Hatching of northern fowl mite eggs held at different temperatures and humidities. J Parasitol 71:122–124. https://doi.org/10.2307/3281992
da Fonseca F (1947) A monograph of the genera and species of Macronyssidae Oudemans, 1936 (synom.: Liponissidae Vitzthum, 1931) (Acari). Proc Zool Soc Lond 118:249–334
Daghir NJ (2008) Poultry production in hot climates. Cromwell Pres, Trowbrige
de Figuereido SM, Guimaraes JH, Gama NMSQ (1993) Biologia e ecologia de malófagos (Insecta: Phthiraptera) em aves de postura de granjas industriais. Rev Bras Parasitol Vet 2:45–51
DeVaney JA (1986) Effects of different feather lengths in the vent area of White Leghorn hens on northern fowl mite populations. Poult Sci 65:452–456. https://doi.org/10.3382/ps.0650452
Devaney JA (1979) The effects of the northern fowl mite, Ornithonyssus sylivarium, on egg production and body weight of caged white Leghorn hens. Poult Sci 58:191–194
DeVaney JA, Beerwinkle KR (1980) A nonchemical method of controlling the northern fowl mite, Ornithonyssus sulviarum (Canestrini and Fanzago), on caged White Leghorn hens. Poult Sci 59:1226–1228. https://doi.org/10.3382/ps.0591226
DeVaney JA, Ziprin RL (1980) Detection and correlation of immune responses in White Leghorn chickens to northern fowl mite, Ornithonyssus sylviarum (Canestrini and Fanzago), Populations. Poult Sci 59:34–37
do Carmo Rezende L, Martins NRDS, Teixeira CM et al (2016) Epidemiological aspects of lice (Menacanthus species) infections in laying hen flocks from the State of Minas Gerais Brazil. Br Poult Sci 57:44–50. https://doi.org/10.1080/00071668.2015.1127893
Doti F, Muzureta A (1989) Ensayo a campo con flumetrina pour-on en Argentina contra ácaros de la subfamilia Dermanyssinae – nuevo método de control de ectoparásitos en la gallina. Vet Argent 6:122
Faccini JLH, Massard CL (1974) Nota sobre a ocorrência de Ornithonyssus sulviarum (Canestrini & Fanzago) (Mesostigmata: Mascronyssidae) em Gallus gallus no Brasil. Arq Univ Fed Rural Rio De Janeiro 4:39–40
Freire J (1968) Fauna parasitária riograndense III. Coelho, cobaia, galinha doméstica, galinha d’Angola, peru, pombo, avestruz. Rev Med Vet São Paulo 3:251–267
Graham AL (2008) Ecological rules governing helminth-microparasite coinfection. Proc Natl Acad Sci U S A 105:566–570. https://doi.org/10.1073/pnas.0707221105
Halbritter DA, Mullens BA (2011) Responses of Ornithonyssus sylviarum (Acari: Macronyssidae) and Menacanthus stramineus (Phthiraptera: Menoponidae) to gradients of temperature, light, and humidity, with comments on microhabitat selection on chickens. J Med Entomol 48:251–261. https://doi.org/10.1603/ME10198
Hall ARD, Gross WB (1975) Effect of social stress and inherited plasma corticosterone levels in chickens on populations of the Northern fowl mite, Ornithonyssus sylviarum. J Parasitol 61:1096–1100
Hall RD, Gross WB, Turner EC (1979) Population development of Ornithonyssus sylviarum (Canestrini and Fanzago) on Leghorn roosters inoculated with steroids and subjected to extremes of social interaction. Vet Parasitol 5:287–297
Hall RD, Turner EC, Gross WB (1978) Effect of cage densities on northern fowl mite populations in commercial caged-layer operations. Poult Sci 57:564–566
Horn TB, Granich J, Körbes JH et al (2018) Mite fauna (Acari) associated with the poultry industry in different laying hen management systems in Southern Brazil: a species key. Acarologia 58:140–158. https://doi.org/10.24349/acarologia/20184233
Kells SA, Surgeoner GA (1996) Dispersion of northern fowl mites, Ornithonyssus sylviarum, between poultry facilities via infested eggs from layer and breeder flocks. J Agric Urban Entomol 13:265–274
Kells SA, Surgeoner GA (1997) Sources of northern fowl mite (Ornithonyssus sylviarum) infestation in Ontario egg production facilities. J Appl Poult Res 6:221–228. https://doi.org/10.1093/japr/6.2.221
Knee W, Proctor H (2007) Host records for Ornithonyssus sylviarum (Mesostigmata: Macronyssidae) from birds of North America (Canada, United States, and Mexico). J Med Entomol 44:150–154. https://doi.org/10.1603/0022-2585(2007)44
Krantz GW (1978) A manual of acarology. Oregon State University, Corvellis
Lareschi M, Cicuttin GL, De Salvo MN et al (2017) The tropical fowl mite Ornithonyssus bursa (Acari: Mesostigmata: Macronyssidae) parasitizing the European starling Sturnus vulgaris (Aves: Passeriformes: Sturnidae), an invasive bird in central Argentina. An approach to the bacterial fauna of this mite. Rev Mex Biodiversidad 88:454–458. https://doi.org/10.1016/j.rmb.2017.03.022
Lemke LA, Kissam JB (1986) The status of northern fowl mite research: how far have we come? J Agric Entomol 3:255–264
Marín-Gómez SY, Benavides-Montaño JA (2007) Parásitos en aves domésticas (Gallus domesticus) en el Noroccidente de Colombia. Vet Zootec 1:43–51
Mascarenhas CS, Coimbra MAA, Müller G, Brum JGW (2009) Ocorrência de Ornithonyssus bursa (Berlese, 1888) (Acari: Macronyssidae) em flhotes de Megascops choliba (orujinha-do-mato) e Pitangus sulphuratus (bem-te-vi), no Rio Grande do Sul, Brasil. Rev Bras Parasitol Vet 18:69–70. https://doi.org/10.4322/rbpv.01804013
McCulloch JB, Jeb P, Hinkle NC et al (2019) Genetic structure of northern fowl mite (Mesostigmata : Macronyssidae) populations among layer chicken flocks and local house sparrows (Passeriformes: Passeridae). J Med Entomol:1–9.https://doi.org/10.1093/jme/tjz136
McCulloch JB, Owen JP (2012) Arrhenotoky and oedipal mating in the northern fowl mite (Ornithonyssus sylviarum) (Acari: Gamasida: Macronyssidae). Parasit Vectors 5:281. https://doi.org/10.1186/1756-3305-5-281
Miller WV, Price FC (1977) The avian mite, Ornithonyssus sylviarum, on mammalian hosts with references to transmission to poultry. J Parasitol 63:417. https://doi.org/10.2307/3279990
Mullens BA, Hinkle NC, Szijj CE (2000) Monitoring northern fowl mites (Acari: Macronyssidae) in caged laying hens: feasibility of an egg-based sampling system. J Econ Entomol 93:1045–1054
Mullens BA, Owen JP, Kuney DR et al (2009) Temporal changes in distribution, prevalence and intensity of northern fowl mite (Ornithonyssus sylviarum) parasitism in commercial caged laying hens, with a comprehensive economic analysis of parasite impact. Vet Parasitol 160:116–133. https://doi.org/10.1016/j.vetpar.2008.10.076
Mullens BA, Velten RK, Hinkle NC et al (2004) Acaricide resistance in northern fowl mite (Ornithonyssus sylviarum) populations on caged layer operations in southern California. Poult Sci 83:365–374. https://doi.org/10.1093/ps/83.3.365
Murillo AC, Mullens BA (2017) A review of the biology, ecology, and control of the northern fowl mite, Ornithonyssus sylviarum (Acari: Macronyssidae). Vet Parasitol 246:30–37. https://doi.org/10.1016/j.vetpar.2017.09.002
Nakamae H, Kishi S, Fujisaki K et al (1996) Effect of trimming feathers off abdominal and crural tracts of the hen on parasitism of mites. Jpn Poult Sci 33:377–382
Oliveira TM, Teixeira CM, Rezende LC et al (2020) Epidemiologia e avaliação de risco associado à presença de ácaros hematófagos em galpões de granjas avícolas de postura. Arq Bras Med Vet Zootec 72:2148–2156
Oppliger A, Clobert J, Lecomte J et al (1998) Environmental stress increases the prevalence and intensity of blood parasite infection in the common lizard Lacerta vivipara. Ecol Lett 1:129–138. https://doi.org/10.1046/j.1461-0248.1998.00028.x
Owen JP, Delany ME, Mullens BA (2008) MHC haplotype involvement in avian resistance to an ectoparasite. Immunogenetics 60:621–631. https://doi.org/10.1007/s00251-008-0314-2
Radovsky FJ (2010) Revision of genera of the parasitic mite family Macronyssidae. Indira Publishing House, West Bloomfield
Reeves WC, Hammon WM, Doetschmann WH et al (1955) Studies on mites as vectors of western equine and St. Louis encephalitis viruses in California. Am J Trop Med Hyg 4:90–105
Reis J, Reis ASS, Nóbrega P (1934) Moléstias de aves observadas em Sao Paulo. Arq Inst Biol 5:41–49
Richner H, Heeb P (1995) Are clutch in birds and brood size patterns shaped by ectoparasites? Oikos 73:435–441. https://doi.org/10.2307/3545973
Santillán MÁ, Grande JM, Liébana MS et al (2015) New hosts for the mite Ornithonyssus bursa in Argentina. Med Vet Entomol 29:439–443. https://doi.org/10.1111/mve.12129
Serafini PS, Anjos LD, Arzua M et al (2003) First report of Ornithonyssus sylviarum (Acari: Macronyssidae) on black vulture (Coragyps atratus) nestlings from Brazil. Rev Bras Parasitol Vet 12:92–93
Sikes RK, Chamberlain RW (1954) Laboratory observations on three species of bird mites. J Parasitol 40:691–697
Teixeira CM, de Oliveira TM, Soriano-Araújo A et al (2020) Ornithonyssus sylviarum (Acari: Macronyssidae) parasitism among poultry farm workers in Minas Gerais State, Brazil. Ciencia Rural 50:1–7. https://doi.org/10.1590/0103-8478cr20190358
Téllez ML, Sordo C, Ruiz A et al (2008) Dermatosis por ácaros de palomas. Primer reporte de la presencia de Ornithonyssus sylviarum en el Perú. Folia Dermatol Peru 19:63–68
Trivedi MC, Rawat BS, Saxena AK (1991) The distribution of lice (Phthiraptera) on poultry (Gallus domesticus). Int J Parasitol 21:247–249. https://doi.org/10.1016/0020-7519(91)90016-Z
Tucci EC, Guimarães JH, Bruno TV et al (1998) Ocorrencia de ácaros hematófagos em aviários de postura no estado de Sao Paulo. Rev Bras Parasitol Vet 7:71–78
Valiente Moro C, Chauve C, Zenner L (2005) Vectorial role of some dermanyssoid mites (Acari, Mesostigmata, Dermanyssoidea). Parasite 12:99–109
Vas Z (1935) Ectoparasitas de animaes domesticos observados no estado de S. Paulo. Arq Inst Biol 6:29–33
Vezzoli G, Mullens BA, Mench JA (2015) Relationships between beak condition, preening behavior and ectoparasite infestation levels in laying hens. Poult Sci 94:1997–2007. https://doi.org/10.3382/ps/pev171
Acknowledgements
We would like to thank the owners of the poultry farms for giving us permission to use their flocks to conduct this study. We would also like to thank Valeria Corbalán and Silvina Sorroche for the assistance during the field work and Exequiel Furlan for creating the map with field site locations.
Funding
This study was funded by the Argentine Council for Research and Technology, CONICET (www.conicet.gob.ar, Grant No. PIP 11220130100561CO), and by Universidad Autónoma de Entre Ríos (Res. 370–15).
Author information
Authors and Affiliations
Contributions
All authors read and approved the final manuscript.
Idea of article by Pablo M. Beldomenico; data collection by Sofia I. Arce, Agustín Fasano, Claudia Sosa, Micaela Gomez, and Leandro R. Antoniazzi; draft preparation by Sofia I. Arce and Pablo M. Beldomenico; review and editing by all authors; and funding acquisition by Pablo M. Beldomenico and Martín A. Quiroga.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no competing interests.
Additional information
Section Editor: Elizabeth Marie Warburton
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Arce, S.I., Antoniazzi, L.R., Fasano, A.A. et al. Factors associated with prevalence and intensity of the northern fowl mite (Ornithonyssus sylviarum) in commercial poultry farms of Argentina. Parasitol Res 121, 1281–1293 (2022). https://doi.org/10.1007/s00436-022-07484-w
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00436-022-07484-w