Skip to main content
SpringerLink
Log in

Molecular characterization and phylogenetic analysis of Argas persicus (Oken, 1818) (Acari: Argasidae) from domestic birds in eastern Algeria

  • Research
  • Published:
Parasitology Research Aims and scope Submit manuscript

Abstract

Argas persicus (the fowl tick) is a species of soft tick commonly associated with poultry farms. It has a wide geographic distribution and colonizes different climate regions. Morphological identification of A. persicus has been reported worldwide, but genetic data regarding its molecular characterization is limited. The present study provides data for morphological identification and genetic characterization of A. persicus collected from domestic birds in traditional farms from east Algeria (Setif region). Additionally, A. persicus samples originating from Gansu province in China were included for comparative molecular study. In total, 1518 ticks collected from 30 infested farms were examined and morphologically identified as A. persicus. Furthermore, the 14 tick samples obtained from China were morphologically identified as A. persicus. Molecular analysis of 30 ticks from Algeria (one tick from each infested farm) and the 14 Chinese samples based on PCR, sequencing, and phylogenetic analysis of three mitochondrial genetic markers (16S rRNA, 12S rRNA, and cox1) confirmed morphological results where all samples belonged to the A. persicus group. However, phylogenetic analysis showed that all Algerian samples and two Chinese samples belong to A. persicus sensu stricto (s.s.), while the remaining Chinese samples represented A. persicus sensu lato (s.l.) (divergent lineage). The present study confirms the occurrence of A. persicus s.s. both in Algeria and China, as well as provides novel molecular data for a distinct Chinese lineage of A. persicus.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Data availability

The tick specimens are in the LCD collection at Bundeswehr Institute of Microbiology.

References

  • Apanaskevich DA, Horak IG, Matthee CA, Matthee S (2011) A new species of Ixodes (Acari: Ixodidae) from South African mammals. J Parasitol 3:389–398

    Article  Google Scholar 

  • Beati L, Keirans JE (2001) Analysis of the systematic relationships among ticks of the genera Rhipicephalus and Boophilus (Acari: Ixodidae) based on mitochondrial 12S ribosomal DNA gene sequences and morphological characters. J Parasitol 87:32–48

    Article  CAS  Google Scholar 

  • Beati L, Klompen H (2019) Phylogeography of ticks (Acari: Ixodida). Annu Rev Entomol 64:379–397

    Article  CAS  Google Scholar 

  • Boucheikhchoukh M, Laroche M, Aouadi A, Dib L, Benakhla A, Raoult D, Parola P (2018) MALDI-TOF MS identification of ticks of domestic and wild animals in Algeria and molecular detection of associated microorganisms. Comp Immunol Microbiol Infect Dis 57:39–49

    Article  Google Scholar 

  • Burger TD, Shao R, Labruna MB, Barker SC (2014) Molecular phylogeny of soft ticks (Ixodida: Argasidae) inferred from mitochondrial genome and nuclear rRNA sequences. Ticks Tick-Borne Dis 5:195–207

    Article  Google Scholar 

  • Black WC IV, Klompen JSH, Keirans JE (1997) Phylogenetic relationships among tick subfamilies (Ixodida: Ixodidae: Argasidae) based on the 18S nuclear rDNA gene. Mol Phylogenet Evol 7:129–144

    Article  CAS  Google Scholar 

  • Black WC IV, Piesman J (1994) Phylogeny of hard- and soft-tick taxa (Acari: Ixodida) based on mitochondrial 16S rDNA sequences. Proc Natl Acad Sci 91:10034–10038

    Article  CAS  Google Scholar 

  • Camicas JL, Morel P-C (1977) Position systématique et classification des tiques (Acarida: Ixodida). Acarologia 18:410–420

    Google Scholar 

  • Camicas JL, Hervy JP, Adam F, Morel P-C (1998) The ticks of the world. Nomenclature, described stages, hosts, distribution (Acarida: Ixodida). Orstom, Paris

    Google Scholar 

  • Clifford CM, Kohls GM, Sonenshine DE (1964) The systematics of the subfamily Ornithodorinae (Acarina: Argasidae). I. The genera and subgenera. Ann Entomol Soc Am 57:429–437

    Article  Google Scholar 

  • Chitimia L, Lin RQ, Cosoroaba I, Wu XY, Song HQ, Yuan ZG, Zhu XQ (2010) Genetic characterization of ticks from southwestern Romania by sequences of mitochondrial cox1 and nad5 genes. Exp Appl Acarol 52:305–311

    Article  Google Scholar 

  • Chen YY, Gao Y, Sun MQ, Wu TT, Chang QC (2020) Complete mitochondrial genome of Argas persicus (Ixodida: Argasidae) isolate China. Mitochondrial DNA Part B 5:1251–1252

    Article  Google Scholar 

  • Chen Z, Liu J (2022) A review of argasid ticks and associated pathogens of China. Front Vet Sci 9:865664

    Article  Google Scholar 

  • Dabert M, Dabert J, Siuda K (1999) Species validity of the soft-tick Argas polonicus (Acari: Argasidae) based on 16S rDNA sequence analysis. In: Bruin J, van der Geest LPS, Sabelis MW (eds) Ecology and Evolution of the Acari Series Entomologica, 55 Springer: Dordrecht. https://doi.org/10.1007/978-94-017-1343-6_58

  • Estrada-Peña A, Mangold AJ, Nava S, Venzal JM, Labruna M, Guglielmone AA (2010) A review of the systematics of the tick family Argasidae (Ixodida). Acarologia 50:317–333

    Article  Google Scholar 

  • Estrada-Peña A, Kleinerman G, Baneth G (2017a) Genus Argas Latreille, 1795. In: Estrada-Peña A, Mihalca AD, Petney TN (eds) Ticks of Europe and North Africa: a guide to species identification. Springer, Cham, pp 13–14

  • Estrada-Peña A, Kleinerman G, Baneth G (2017b) Genus Ornithodoros Koch, 1844. In: Estrada-Peña A, Mihalca AD, Petney TN (eds), Ticks of Europe and North Africa: a guide to species identification. Springer, Cham, pp 41–43

  • Feng J, Wu M, Wulan HT, Zhang J, Renbatu N, Riletu G (2019) Identification of two genotypes of Argas persicus and associated Rickettsia-specific genes from different regions of Inner Mongolia. J Parasitol 105:92–101

    Article  CAS  Google Scholar 

  • Filippova NA (1966) Argasid ticks (Argasidae). Zoologicheskogo Institut Akademii Nauk SSSR, Moscow-Leningrad (in Russian)

    Google Scholar 

  • Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol 3:294–299

    CAS  Google Scholar 

  • Gabaj MM, Awan MAQ, Beesley WN (1992) A survey of ticks on farm animals in Libya. Ann Trop Med Parasitol 86:543–548

    Article  CAS  Google Scholar 

  • Guglielmone AA, Robbins RG, Apanaskevich DA, Petney TN, Estrada-Peña A, Horak IG, Shao R, Barker SC (2010) The Argasidae, Ixodidae and Nuttalliellidae (Acari: Ixodida) of the world: a list of valid species names. Zootaxa 2528:1–28

    Article  Google Scholar 

  • Halos L, Jamal T, Vial L, Maillard R, Suau A, Le Menach A, Boulouis HJ, Vayssier-Taussat M (2004) Determination of an efficient and reliable method for DNA extraction from ticks. Vet Res 35:709–713

    Article  CAS  Google Scholar 

  • Hoogstraal H (1985) Argasid and nuttalliellid ticks as parasites and vectors. Adv Parasitol 24:135–238

    Article  CAS  Google Scholar 

  • Hoogstraal H, Kohls GM (1960) Observations on the subgenus Argas (Ixodoidea, Argasidae, Argas) 1. Study of A. reflexus reflexus (Fabricius, 1794), the European bird argasid. Ann Entomol Soc Am 53:611–618

    Article  Google Scholar 

  • Hosseini-Chegeni A, Tavakoli M, Telmadarraiy Z, Faghihi F (2020) Molecular detection of spotted fever group Rickettsia (Rickettsiales: Rickettsiaceae) in ticks of Iran. Arch Razi Inst 75:317–325

    CAS  Google Scholar 

  • Kaboudi K, Romdhane RB, Salem AB, Bouzouaia M (2019) Occurrence of ectoparasites in backyard domestic chickens (Gallus gallus domesticus) in the northeast of Tunisia. J Anim Health Prod 7:92–98

    Google Scholar 

  • Katoh K, Misawa K, Kuma K, Miyata T (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res 30:3059–3066

    Article  CAS  Google Scholar 

  • Klompen JSH, Oliver JH (1993) Systematic relationships in the soft ticks (Acari: Ixodida: Argasidae). Syst Entomol 18:313–331

    Article  Google Scholar 

  • Kumar S, Stecher G, Tamura K (2016) MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874

    Article  CAS  Google Scholar 

  • Labuda M, Nuttall PA (2004) Tick-borne viruses. Parasitology 129:S221–S245

    Article  CAS  Google Scholar 

  • Lafri I, Benredjem W, Neffah-Baaziz F, Lalout R, Abdelouahed K, Gassen B, Bakhouch S, Chergui M, Karakellah M, Adjmi-Hamoudi H, Bitam I (2018) Inventory and update on argasid ticks and associated pathogens in Algeria. New Microbe New Infect 23:110–114

    Article  CAS  Google Scholar 

  • Lafri I, El Hamzaoui B, Bitam I, Leulmi H, Lalout R, Mediannikov O, Chergui M, Karakellah M, Raoult D, Parola P (2017) Detection of relapsing fever Borrelia spp., Bartonella spp. and Anaplasmataceae bacteria in argasid ticks in Algeria. PloS Negl Trop Dis 11:e0006064

    Article  Google Scholar 

  • Loftis AD, Reeves WK, Szumlas DE, Abbassy MM, Helmy IM, Moriarity JR, Dasch GA (2006) Rickettsial agents in Egyptian ticks collected from domestic animals. Exp Appl Acarol 40:67–81

    Article  Google Scholar 

  • Mans BJ, Featherston J, Kvas M, Pillay KA, de Klerk DG, Pienaar R, de Castro MH, Schwan TG, Lopez JE, Teel P, Pérez de León AA, Sonenshine DE, Egekwu NI, Bakkes DK, Heyne H, Kanduma EG, Nyangiwe N, Bouattour A, Latif AA (2019) Argasid and ixodid systematics: implications for soft tick evolution and systematics, with a new argasid species list. Ticks Tick-Borne Dis 10:219–240

    Article  Google Scholar 

  • Mans BJ, Kelava S, Pienaar R, Featherston J, de Castro MH, Quetglas J, Reeves WK, Durden LA, Miller MM, Laverty TM, Shao R, Takano A, Kawabata H, Moustafa MAM, Nakao R, Matsuno K, Greay TL, Evasco KL, Barker D, Barker SC (2021) Nuclear (18S–28S rRNA) and mitochondrial genome markers of Carios (Carios) vespertilionis (Argasidae) support Carios Latreille, 1796 as a lineage embedded in the Ornithodorinae: re-classification of the Carios sensu Klompen and Oliver (1993) clade into its respective subgenera. Ticks Tick-Borne Dis 12:101688

    Article  Google Scholar 

  • Manzano-Román R, Díaz-Martín V, de la Fuente J, Pérez-Sánchez R (2012) Soft ticks as pathogen vectors: distribution. INTECH Open Access Publisher, Surveillance and Control

    Google Scholar 

  • Muñoz-Leal S, Venzal JM, Nava S, Reyes M, Martins TF, Leite RC, Vilela VLR, Benatti HR, Ríos-Rosas D, Barros-Battesti DM, González-Acuña D, Labruna MB (2018) The geographic distribution of Argas (Persicargas) miniatus and Argas (Persicargas) persicus (Acari: Argasidae) in America, with morphological and molecular diagnoses from Brazil, Chile and Cuba. Ticks Tick-Borne Dis 9:44–56

    Article  Google Scholar 

  • Nahal A, Righi S, Boucheikhchoukh M, Benakhla A (2021) Prevalence of ectoparasites in free-range backyard chicken flocks in northeast Algeria. Veterinarska Stanica 52:693–702

    Article  Google Scholar 

  • Nava S, Guglielmone AA, Mangold AJ (2009) An overview of systematics and evolution of ticks. Front Biosci 14:2857–2877

    Article  CAS  Google Scholar 

  • Norris DE, Klompen JSH, Black WC IV (1999) Comparison of the mitochondrial 12S and 16S ribosomal DNA genes in resolving phylogenetic relationships among hard ticks (Acari: Ixodidae). Ann Entomol Soc Am 92:117–129

    Article  CAS  Google Scholar 

  • Nuttall PA, Jones LD, Labuda M, Kaufman WR (1994) Adaptations of arboviruses to ticks. J Med Entomol 31:1–9

    Article  CAS  Google Scholar 

  • Ouchene N, Nebbak A, Ouchene-Khelifi NA, Dahmani A, Zeroual F, Khelef D, Bitam I, Benakhla A, Parola P (2020) Molecular detection of avian spirochete Borrelia anserina in Argas persicus ticks in Algeria. Comp Immunol Microbiol Infect Dis 68:101408

    Article  Google Scholar 

  • Pader V, Nikitorowicz Buniak J, Abdissa A, Adamu H, Tolosa T, Gashaw A, Cutler RR, Cutler SJ (2012) Candidatus Rickettsia hoogstraalii in Ethiopian Argas persicus ticks. Ticks Tick-Borne Dis 3:338–345

    Article  Google Scholar 

  • Pantaleoni RA, Baratti M, Barraco L, Contini C, Cossu CS, Filippelli MT, Loru L, Romano M (2010) Argas (Persicargas) persicus (Oken, 1818) (Ixodida: Argasidae) in Sicily with considerations about its Italian and West-Mediterranean distribution. Parasite 17:349–355

    Article  CAS  Google Scholar 

  • Petney TN, Andrews RH, McDiarmid LA, Dixon BR (2004) Argas persicus sensu stricto does occur in Australia. Parasitol Res 93:296–299

    Article  CAS  Google Scholar 

  • Pfäffle MP, Petney TN (2017) Argas persicus (Oken, 1818). In: Estrada-Peña A, Mihalca AD, Petney TN (eds), Ticks of Europe and North Africa: a guide to species identification. Springer, Cham, pp 15–19

  • Palomar AM, Veiga J, Portillo A, Santibáñez S, Václav R, Santibáñez P, Oteo JA, Valera F (2021) Novel genotypes of Nidicolous Argas ticks and their associated microorganisms from Spain. Front Vet Sci 8:637837

    Article  Google Scholar 

  • Pospelova-Shtrom MV (1969) On the system of classification of ticks of the family Argasidae Can., 1890. Acarologia 11:1–22

    CAS  Google Scholar 

  • Rehácek J, Urvölgyi J, Kovácová E (1977) Massive occurrence of rickettsiae of the spotted fever group in fowl tampan, Argas persicus, in the Armenian S.S.R. Acta Virol 21:431–438

    Google Scholar 

  • Sang C, Yang M, Xu B, Liu G, Yang Y, Kairullayev K, Bauyrzhan O, Hazihan W, Hornok S, Wang Y (2021) Tick distribution and detection of Babesia and Theileria species in Eastern and Southern Kazakhstan. Ticks Tick-Borne Dis 12:101817

    Article  Google Scholar 

  • Sheng J, Jiang M, Yang M, Bo X, Zhao S, Zhang Y, Wureli H, Wang B, Tu C, Wang Y (2019) Tick distribution in border regions of Northwestern China. Ticks Tick- Borne Dis 10:665–669

    Article  Google Scholar 

  • Trifinopoulos J, Nguyen LT, von Haeseler A, Minh BQ (2016) W-IQ-TREE: A fast online phylogenetic tool for maximum likelihood analysis. Nucleic Acids Res 44:W232–W235

    Article  CAS  Google Scholar 

  • Vermeil C, Marjolet M, Chastel C (1996) Argas and arbovirus update. Bull Soc Pathol Exot 89:363–365

    CAS  Google Scholar 

  • Walker AR, Bouattour A, Camicas J-L, Estrada-Peña A, Horak IG, Latif AA, Pegram RG, Preston PM (2003) Ticks of domestic animal in Africa: a guide to identification of species. Biosci Rep, Edinburgh

    Google Scholar 

  • Yavari S, Nabian S, Ebrahimzade Abkooh E, Shayan P, Shokrani H (2019) Genetic characterization of Argas persicus from Iran by sequencing of mitochondrial cytochrome oxidase I (cox1) and 16S rRNA genes. Iran J Vet Med 13:45–57

    Google Scholar 

  • Zahid H, Muñoz-Leal S, Khan MQ, Alouffi AS, Labruna MB, Ali A (2021) Life cycle and genetic identification of Argas persicus infesting domestic fowl in Khyber Pakhtunkhwa. Pakistan Front Vet Sci 8:664731

    Article  Google Scholar 

Download references

Acknowledgements

The authors gratefully thank the owners of the chicken farms for their help in tick sampling.0

Author information

Authors and Affiliations

  1. Laboratory of Exploration and Valorization of Steppic Ecosystems, Faculty of Nature and Life Sciences, University of Djelfa, Moudjbara Road, BP 3117, Djelfa, Algeria

    Amira Rahmani & AbdElkarim Laatamna

  2. Hebei Key Laboratory of Animal Physiology, Biochemistry and Molecular Biology, College of Life Sciences, Hebei Normal University, Shijiazhuang, 050016, China

    Zhijun Yu

  3. Institut Des Sciences Vétérinaires, Université de Blida 1, 09000, Blida, Algeria

    Ismail Lafri

  4. Faculty of Nature and Life Sciences, University of Laghouat, Ghardaïa Road, BP 37, Laghouat, Algeria

    Zakaria Herrada

  5. Bundeswehr Institute of Microbiology, Munich, Germany

    Lidia Chitimia-Dobler

  6. Gertrud Theiler Tick Museum, Agricultural Research Council–Onderstepoort Veterinary Research, Pretoria, South Africa

    Deon K. Bakkes

Authors
  1. Amira Rahmani
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. AbdElkarim Laatamna
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Zhijun Yu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ismail Lafri
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Zakaria Herrada
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Lidia Chitimia-Dobler
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Deon K. Bakkes
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Amira Rahmani, AbdElkarim Laatamna, Zakaria Herrada, and Zhijun Yu collected and provided the ticks. Amira Rahmani, Ismail Lafri, and Lidia Chitimia-Dobler did morphological identification. Lidia Chitimia-Dobler did DNA extraction and molecular tests. Lidia Chitimia-Dobler prepared Figs. 2 and 3. AbdElkarim Laatamna and Amira Rahmani prepared Fig. 1. Deon K. Bakkes did the genetic analysis and sequence submission and prepared Figs. 4, 5, and 6. AbdElkarim Laatamna, Amira Rahmani, Lidia Chitimia-Dobler, and Deon K. Bakkes wrote the manuscript. All authors read and reviewed the final version of the manuscript.

Corresponding author

Correspondence to AbdElkarim Laatamna.

Ethics declarations

Ethics approval

Not applicable.

Consent to participate

Not applicable.

Consent for publication

All authors gave their consent for publication.

Competing interests

The authors declare no competing interests.

Additional information

Section Editor: Van Lun Low

Publisher's note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Lidia Chitimia-Dobler and Deon K. Bakkes share the last author position

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.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Rahmani, A., Laatamna, A., Yu, Z. et al. Molecular characterization and phylogenetic analysis of Argas persicus (Oken, 1818) (Acari: Argasidae) from domestic birds in eastern Algeria. Parasitol Res 122, 275–284 (2023). https://doi.org/10.1007/s00436-022-07727-w

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-022-07727-w

Keywords

Search

Navigation