Particle and Fibre Toxicology | |
The enigma of the dog mummy from Ancient Egypt and the origin of ‘Rhipicephalus sanguineus’ | |
Filipe Dantas-Torres3  Cecile Callou1  Alessio Giannelli2  Jean-Bernard Huchet1  Domenico Otranto2  | |
[1] UMR 7209 du CNRS, Archéozoologie, Archéobotanique, Muséum National d’Histoire Naturelle, Paris, France;Department of Veterinary Medicine, University of Bari, Valenzano, Bari, Italy;Department of Immunology, Aggeu Magalhães Research Centre, Oswaldo Cruz Foundation, Recife, Pernambuco 50670420, Brazil | |
关键词: Origins; Archeoparasitology; Dog mummy; Rhipicephalus sanguineus; Tick; | |
Others : 822984 DOI : 10.1186/1756-3305-7-2 |
|
received in 2013-12-06, accepted in 2013-12-21, 发布年份 2014 | |
【 摘 要 】
Background
Ticks belonging to the Rhipicephalus sanguineus group are amongst the most important vectors of pathogenic microorganisms to dogs and humans. However, the taxonomy of this species group is still the subject of debate, especially because there is no type specimen or reliable morphological description for Rhipicephalus sanguineus sensu stricto. Recently, a comprehensive morphological and genetic study on representative tick specimens from Europe, Africa, Americas, and Oceania, revealed the existence of at least four morphologically and genetically distinct species under the name ‘R. sanguineus’ infesting dogs from different countries.
Methods
Herein, we examined morphologically tick specimens retrieved on a dog mummy from Ancient Egypt (ca. 1st century – 4th century A.D.). The dog mummy and associated ticks were found during an archaeological expedition conducted in El Deir.
Results
Scanning electron micrographs allowed us to assess their identity as belonging to the R. sanguineus group. In addition on the basis of the scutal punctation pattern, spiracular plates, width of dorsal tail of spiracular plates relative to the adjacent festoon, female genital aperture, male adanal plates and accessory shields, these ticks were tentatively identified as Rhipicephalus sp. II (=temperate species).
Conclusions
It can be concluded that R. sanguineus group ticks have infested dogs living in the Mediterranean region since ancient times. This finding represents the oldest record of ticks on any animal species and adds a new piece in the complex puzzle regarding tick parasitism on dogs and humans and their role as vectors of pathogens.
【 授权许可】
2014 Otranto et al.; licensee BioMed Central Ltd.
【 预 览 】
Files | Size | Format | View |
---|---|---|---|
20140712132143238.pdf | 1156KB | download | |
Figure 2. | 105KB | Image | download |
Figure 1. | 94KB | Image | download |
【 图 表 】
Figure 1.
Figure 2.
【 参考文献 】
- [1]Dantas-Torres F, Otranto D: Dogs, cats, parasites, and humans in Brazil: opening the black box. Parasit Vectorsin press
- [2]Otranto D, Dantas-Torres F, Brianti E, Traversa D, Petrić D, Genchi C, Capelli G: Vector-borne helminths of dogs and humans in Europe. Parasit Vectors 2013, 6:16. BioMed Central Full Text
- [3]Dantas-Torres F, Chomel BB, Otranto D: Ticks and tick-borne diseases: a One Health perspective. Trends Parasitol 2012, 28:437-446.
- [4]Dantas-Torres F, Latrofa MS, Annoscia G, Giannelli A, Parisi A, Otranto D: Morphological and genetic diversity of Rhipicephalus sanguineus sensu lato from the New and Old Worlds. Parasit Vectors 2013, 6:213. BioMed Central Full Text
- [5]Guglielmone AA, Robbins RG, Apanaskevich DA, Petney TN, Estrada-Peña A, Horak IG: Comments on controversial tick (Acari: Ixodida) species names and species described or resurrected from 2003 to 2008. Exp Appl Acarol 2009, 48:311-327.
- [6]Neumann LG: Ixodidae. Berlin: Das Tierreich; 1911.
- [7]Camicas JL, Hervy JP, Adam F, Morel PC: Les tiques du monde. Nomenclature, stades décrits, hôtes, répartition (Acarida, Ixodida). Paris: Éditions de l’Orstom; 1998.
- [8]Walker JB, Keirans JE, Horak IG: The Genus Rhipicephalus (Acari, Ixoidae). A Guide to the Brown Ticks of the World. Cambridge, UK: Cambridge Univ. Press; 2000.
- [9]Gray J, Dantas-Torres F, Estrada-Peña A, Levin M: Systematics and ecology of the brown dog tick, Rhipicephalus sanguineus. Ticks Tick Borne Dis 2013, 4:171-180.
- [10]Oliveira PR, Bechara GH, Denardi SE, Saito KC, Nunes ET, Szabó MP, Mathias MI: Comparison of the external morphology of Rhipicephalus sanguineus (Latreille, 1806) (Acari: Ixodidae) ticks from Brazil and Argentina. Vet Parasitol 2005, 129:139-147.
- [11]Szabó MP, Mangold AJ, João CF, Bechara GH, Guglielmone AA: Biological and DNA evidence of two dissimilar populations of the Rhipicephalus sanguineus tick group (Acari: Ixodidae) in South America. Vet Parasitol 2005, 130:131-140.
- [12]Burlini L, Teixeira KR, Szabó MP, Famadas KM: Molecular dissimilarities of Rhipicephalus sanguineus (Acari: Ixodidae) in Brazil and its relation with samples throughout the world: is there a geographical pattern? Exp Appl Acarol 2010, 50:361-374.
- [13]Moraes-Filho J, Marcili A, Nieri-Bastos FA, Richtzenhain LJ, Labruna MB: Genetic analysis of ticks belonging to the Rhipicephalus sanguineus group in Latin America. Acta Trop 2011, 117:51-55.
- [14]Levin ML, Studer E, Killmaster L, Zemtsova G, Mumcuoglu KY: Crossbreeding between different geographical populations of the brown dog tick, Rhipicephalus sanguineus (Acari: Ixodidae). Exp Appl Acarol 2012, 58:51-68.
- [15]Nava S, Mastropaolo M, Venzal JM, Mangold AJ, Guglielmone AA: Mitochondrial DNA analysis of Rhipicephalus sanguineus sensu lato (Acari: Ixodidae) in the Southern Cone of South America. Vet Parasitol 2012, 190:547-555.
- [16]Latrofa MS, Dantas-Torres F, Annoscia G, Cantacessi C, Otranto D: Comparative analyses of mitochondrial and nuclear genetic markers for the molecular identification of Rhipicephalus spp. Infect Genet Evol 2013, 20C:422-427.
- [17]Reinhard KJ: Archaeoparasitology in North America. Am J Phys Anthropol 1990, 82:145-163.
- [18]Otranto D, Stevens JR, Brianti E, Dorchies P: Human and livestock migrations: a history of bot fly biodiversity in the Mediterranean region. Trends Parasitol 2006, 22:209-213.
- [19]Fry GF: Analysis of fecal material. In The Analysis of Prehistoric Diets. Edited by Gilbert RIJr, Mielke J. Orlando: Academic Press; 1985:127-154.
- [20]Reinhard KJ, Confalonieri UE, Herrmann B, Ferreira LF, Araujo AJG: Recovery of parasite eggs from coprolites and latrines: aspects of paleoparasitological technique. Homo 1998, 37:217-239.
- [21]Gonçalves MLC, Araujon A, Ferreira LF: Human intestinal parasites in the past: new findings and a review. Mem Inst Oswaldo Cruz 2003, 98:103-118.
- [22]Bouchet F, Harter S, Le Bailly M: The state of the art of paleoparasitological research in the old world. Mem Inst Oswaldo Cruz 2003, 98:95-101.
- [23]Araújo A, Reinhard K, Leles D, Sianto L, Iñiguez A, Fugassa M, Arriaza B, Orellana N, Ferreira LF: Paleoepidemiology of intestinal parasites and lice in pre-Columbian America. Rev Chil Hist Nat 2001, 43:303-313.
- [24]Capasso L, Di Tota G: Lice buried under the ashes of Herculaneum. Lancet 1998, 351:992.
- [25]Yvinec JH, Ponel P, Beaucournu JC: Premiers apports archéoentomologiques de l’étude des Puces, Aspects historiques et anthropologiques (Siphonaptera). Bull Soc Ent Fr 2000, 105:419-425.
- [26]Rick FM, Rocha GC, Dittmar K, CoimbraX CE Jr, Reinhard K, Bouchet F, Ferreira LF, Araujo A: Crab louse infestation in pre-Columbian America. J Parasitol 2002, 88:1266-1267.
- [27]Guerra RMSNC, Gazeta GS, Amorim M, Duarte AN, Serra-Freire NM: Ecological analysis of acari recovered from coprolites from archaeological site of northeast Brazil. Mem Inst Oswaldo Cruz 2003, 98:181-190.
- [28]Dittmar K, Mamat U, Whiting M, Goldmann T, Reinhard K, Guillen S: Techniques of DNA-studies on Prehispanic Ectoparasites (Pulex sp., Pulicidae, Siphonaptera) from animal mummies of the Chiribaya culture, Southern Peru. Mem Inst Oswaldo Cruz 2003, 98:53-58.
- [29]Reinhard KJ, Buikstra J: Louse infestation of the Chiribaya culture, Southern Peru: variation in prevalence by age and sex. Mem Inst Oswaldo Cruz 2003, 98:173-179.
- [30]Guerra RMSNC, Duarte AN, Oliveira HH, Mello RP, Serra-Freire NM: The finding of Felicola felis (Mallophaga: Trichodectidae) and exuviae of Amblycera in Felidae coprolites from the archaeological site of Furna do Estrago, Pernambuco state, Brazil. Entomol Vect 2001, 8:395-402.
- [31]Martinson E, Reinhard KJ, Buikstra JE, Dittmar de la Cruz K: Pathoecology of Chiribaya Parasitism. Mem Inst Oswaldo Cruz 2003, 98:195-205.
- [32]Arthur DR: Ticks in Egypt in 1500 B.C.? Nature 1965, 206:1060-1061.
- [33]Huchet JB, Callou C, Lichtentberg R, Dunand F: The dog mummy, the ticks and the louse fly: archaeological report of a severe ectoparasitosis in Ancient Egypt. Int J Paleopathol 2013, 3:165-175.
- [34]Dunand F, Lichtenberg R: Dix ans d’exploration des nécropoles d’El-Deir (oasis de Kharga). Un premier bilan. Chron Egypte 2008, 83:258-288.
- [35]Dunand F, Coudert M, Letellier-Willemin F: Decouverte d’une nécropole chrétienne sur le site d’El-Deir (oasis de Kharga). In Etudes coptes X, Douzième journée d’études (Lyon, 19–21 mai 2005). Edited by Cahiers de la Bibliothèque copte. Paris: Boud’hors A and Louis C; 2008:137-155.
- [36]Dunand F, Heim JL, Lichtenberg R, Brones S, Devaux E, Dussarps L, Letellier-Willemin F, Tallet G: El-Deir Nécropoles II. Les Nécropoles Nord et Nord-Est. Paris: Cybèle; 2012.
- [37]Dunand F, Heim JL, Lichtenberg R, Brones S, Letellier-Willemin F: El-Deir Nécropoles I. La Nécropole Sud. Paris: Cybèle; 2010.
- [38]Callou C, Dunand F, Lichtenberg R: Archaeological and Archaeozoological Study of Dogs from El-Deir. Edited by PalArch’s J Archaeol. Egypt/Egyptol. Cairo, Egypt: Proceeding of International meeting of The Bioarchaeology of Ancient Egypt; 2013:10.
- [39]Filippova NA: Fauna of Russia and Neighbouring Countries. Ixodid Ticks of Subfamily Amblyomminae. Moscow, Russia: Nauka Publishing House; 1997:436.
- [40]Dantas-Torres F: The brown dog tick, Rhipicephalus sanguineus (Latreille, 1806) (Acari: Ixodidae): from taxonomy to control. Vet Parasitol 2008, 152:173-185.
- [41]Otranto D, Dantas-Torres F, Breitschwerdt EB: Managing canine vector-borne diseases of zoonotic concern: part two. Trends Parasitol 2009, 25:228-235.
- [42]Bradfield JF, Vore SJ, Pryor WH Jr: Ehrlichia platys infection in dogs. Lab Anim Sci 1996, 46:565-568.
- [43]Harrus S, Aroch I, Lavy E, Bark H: Clinical manifestations of infectious canine cyclic thrombocytopenia. Vet Rec 1997, 141:247-250.
- [44]Kontos VJ, Koutinas AF: Clinical observations in 15 spontaneous cases of canine babesiosis. Canine Practice 1997, 22:30-34.
- [45]Kordick SK, Breitschwerdt EB, Hegarty BC, Southwick KL, Colitz CM, Hancock SI, Bradley JM, Rumbough R, Mcpherson JT, MacCormack JN: Coinfection with multiple tick-borne pathogens in a Walker Hound kennel in North Carolina. J Clin Microbiol 1999, 37:2631-2638.
- [46]de Caprariis D, Dantas-Torres F, Capelli G, Mencke N, Stanneck D, Breitschwerdt EB, Otranto D: Evolution of clinical, haematological and biochemical findings in young dogs naturally infected by vector-borne pathogens. Vet Microbiol 2011, 149:206-212.
- [47]Otranto D, Dantas-Torres F, Tarallo VD, Ramos RA, Stanneck D, Baneth G, de Caprariis D: Apparent tick paralysis by Rhipicephalus sanguineus (Acari: Ixodidae) in dogs. Vet Parasitol 2012, 188:325-329.