Abstract
The water buffalo (Bubalus bubalis) is an Asian species of bovine which was introduced in Mexico in 1992, as an alternative for milk and meat production. However, little is known about its associated ectoparasites, in particular about their lice. As a part of a project to identify the diversity and prevalence of Anaplasma in cattle and water buffaloes in the state of Veracruz, Mexico, we visited a ranch in the downtown area in which 42 buffaloes were visually inspected for the presence of ectoparasites. Lice were manually recovered, and morphologically identified using taxonomic keys. They were also molecularly identified by the amplification of a fragment of the cytochrome oxidase C subunit I gene (COX1). As a result, we recovered 20 lice from eight animals. All lice were identified as Haematopinus tuberculatus, and the recovered sequences exhibited a similarity of 99.7% with those of the same species deposited in GenBank. Additionally, we detected the presence of Anaplasma marginale in 70% (14/20) of the analysed samples. Our results represent the first record of this exotic ectoparasite for the country.
References
Aguilar-Domínguez M, Romero-Salas D, Sánchez-Montes S, Barradas-Piña F, Rosas-Saito G, Cruz-Romero A, Ibarra-Priego N, Becker I, Lohmeyer KH, Pérez de León A (2018) Occurrence of Amblyomma mixtum on the water buffalo (Bubalus bubalis) in Mexico. Int J Parasitol Parasites Wildl 7:405–408. https://doi.org/10.1016/j.ijppaw.2018.10.005
Batista HR, Sarturi C, Stelmachtchuk FN, Oliveira DR, Morini AC, Gennari SM, Marcili A, Bastos FAN, Barata LES, Minervino AHH (2018) Prevalence and risk factors associated with ectoparasite infestation of buffaloes in an Amazonian ecosystem. Parasit Vectors 11:335. https://doi.org/10.1186/s13071-018-2917-2
Bifulco G, Veneziano V, Cimmino R, Esposito L, Auletta L, Varricchio E, Balestrieri A, Claps S, Campanile G, Neglia G (2015) Effect of pour-on alphacypermethrin on feed intake, body condition score, milk yield, pregnancy rates, and calving-to-conception interval in buffaloes. J Anim Sci 93:1850–1858. https://doi.org/10.2527/jas.2014-8352
Burmeister (1839) Handbuch der Entomologie. 2. Band. Handbuch der Entomologie, 2., Berlin pp XII+1050
Da Silva AS, Lopes LS, Diaz JD, Tonin AA, Stefani LM, Araújo DN (2013) Lice outbreak in buffaloes: evidence of Anaplasma marginale transmission by sucking lice Haematopinus tuberculatus. J Parasitol 99:546–547. https://doi.org/10.1645/GE-3260.1
de la Fuente J, Van Den Bussche RA, Prado TM, Kocan KM (2003) Anaplasma marginale msp1alpha genotypes evolved under positive selection pressure but are not markers for geographic isolates. J Clin Microbiol 41:1609–1616. https://doi.org/10.1128/jcm.41.4.1609-1616.2003
Durden LA (2002) Lice. In: Mullen GR, Durden LA (eds) Medical and veterinary entomology. AcademicPress/Elsevier Science, San Diego, pp 45–63
Durden LA, Musser GG (1994) The sucking lice (Insecta: Anoplura) of the world: a taxonomic checklist with records of mammalian hosts and geographical distributions. Bull Am Mus Nat Hist 218:1–90
Egri B, Piszmán R (2014) Prevalence of Haematopinus tuberculatus in buffalo stocks. Magyar Allatorvosok Lapja 136:59–64
Figueiredo MAP, Silva DF, Manrique WG, Guerra RMSNC (2013) Infestación y distribución de Haematopinus tuberculatus en bubalinos de São Luís, estado do Maranhão, Brasil. Biologist 11:167–172
Hafner MS, Sudman PD, Villablanca FX, Spradling TA, Demastes JW, Nadler SA (1994) Disparate rates of molecular evolution in cospeciation hosts and parasites. Science 265:1087–1090
Khater HF, Ramadan MY, El-Madawy RS (2009) Lousicidal, ovicidal and repellent efficacy of some essential oils against lice and flies infesting water buffaloes in Egypt. Vet Parasitol 164:257–266. https://doi.org/10.1016/j.vetpar.2009.06.011
Kim KC, Pratt HD, Stojanovich CJ (1986) The sucking lice of North America: an illustrated manual for identification. Philadelphia/London: ThePennsylvania State University Press, University Park
McFarland J, Coles GC (2002) Haematopinus tuberculatus on water buffaloes in England. Vet Rec 150:616
Murphy DS, Lee X, Larson SR, Johnson DK, Loo T, Paskewitz SM (2017) Prevalence and distribution of human and tick infections with the Ehrlichia muris-like agent and Anaplasma phagocytophilum in Wisconsin, 2009-2015. Vector Borne Zoonotic Dis 17:229–236. https://doi.org/10.1089/vbz.2016.2055
Neglia G, Veneziano V, De Carlo E, Galiero G, Borriello G, Francillo M, Campanile G, Zicarelli L, Manna L (2013) Detection of Brucella abortus DNA and RNA in different stages of development of the sucking louse Haematopinus tuberculatus. BMC Vet Res 9:236. https://doi.org/10.1186/1746-6148-9-236
Promrangsee C, Khositharattanakool P, Somwang P, Sunantaraporn S, Phumee A, Preativatanyou K, Tawatsin A, Brownell N, Siriyasatien P (2019) The prevalence of Bartonella bacteria in cattle lice collected from three provinces of Thailand. Insects 10:E152. https://doi.org/10.3390/insects10060152
Rawat BS, Trivedi MC, Saxena AK, Kumar A (1992) Incidence of phthirapteran infestation upon the buffaloes of Dehradun (India). Angew Parasitol 33:17–22
Ruiz Buitrago JD, Cardona Zuluaga EA, Berdugo Gutierrez JA, Cardona Arboleda W (2018) Efficacy and safety of topical fipronil 1% and deltamethrin 0.1% in water buffaloes (Bubalus bubalis) naturally infested by Haematopinus tuberculatus. J Buffalo Sci 7:8–12
Sánchez-Montes S, Guzmán-Cornejo C, Ramírez-Corona F, León-Paniagua L (2016) Anoplurans (Insecta: Psocodea: Anoplura) associated with rodents distributed in the neotropical region of Mexico. Rev Mex Bio 87:427–435
Tasawar Z, Bano I, Hayat CS, Lasharim H (2008) Prevalence of lice on buffaloes at private cattle farm. Pak Vet J 28:147–149
Veneziano V, Rinaldi L, Giannetto S, Cringoli G (2003) The first record of Haematopinus tuberculatus on Bubalus bubalis (water buffalo) in Italy. Bubalus bubalis 9:69–75
Veneziano V, Santaniello M, Carbone S, Pennacchio S, Morgoglione ME, Schioppi M, Condoleo R, Cringoli G (2007) Lice (Haematopinus tuberculatus) in water buffalo farms from Central Italy. Ital J Anim Sci 6:926–927
Veneziano V, Neglia G, Cimmino R, Balestrieri A, Rufrano D, Bastianetto E, Santoro M, Gokbulut C (2013) The efficacy and safety of alphacypermethrin as a pour-on treatment for water buffalo (Bubalus bubalis) infested with Haematopinus tuberculatus (Phthiraptera: Haematopinidae). Parasitol Res 112:2907–2912. https://doi.org/10.1007/s00436-013-3462-8
Wirth WW, Marston N (1968) A method for mounting small insects on microscope slides in Canada balsam. Ann Entomol Soc Am 61:783–784
Acknowledgements
We thank the buffalo producers for their collaboration to get this study completed. We are grateful to the staff of the Parasitology Laboratory of the Veterinary School of the State University of Veracruz and the undergraduate students for their support to accomplish this study. The USDA is an equal opportunity provider and employer.
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Ethics approval and consent to participate
This project was approved by the Bioethics and Animal Welfare Commission of the Veterinary and Animal Science School (Facultad de Medicina Veterinaria y Zootecnia) of the State University of Veracruz (Universidad Veracruzana). Consent was obtained from the buffalo producers.
Additional information
Section Editor: Neil Bruce Chilton
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Hernández-Velasco, A., Sánchez-Montes, S., Romero-Salas, D. et al. First record of natural infection with Anaplasma marginale in sucking lice infesting the water buffalo (Bubalus bubalis) in Mexico. Parasitol Res 119, 3853–3856 (2020). https://doi.org/10.1007/s00436-020-06772-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00436-020-06772-7