Occurrence of Ophionyssus natricis (Acari: Macronyssidae) on the captive corn snake, Pantherophis guttatus, (Squamata: Colubridae) in Turkey

Abstract

Exotic snakes may harbour numerous parasites and play an important role in the spreading of parasites. Ophionyssus natricis (Gervais) (Acari: Macronyssidae) has been found in natural conditions on a wide variety of snakes in Africa, but this mite has been distributed by exotic pet trade in various parts of the world. In the present study, O. natricis was reported on the captive corn snake, Pantherophis guttatus (L.) (Squamata: Colubridae), in Turkey, for the first time. Male and protonymph stage of O. natricis were also first time reported in Turkey. In addition, some setal variations in the pygidial shield of protonymphs were documented.

Keywords

• Infestation
• parasitic mites
• pest animal
• Reptilia

References

1. Altınok-Yipel, F. 2014. The infestation of ectoparasites (Hirstiella spp.) treatment with ivermectin solition in a green iguana: case report. Kocatepe Veterinary Journal, 7: 85-87. doi: 10.5578/kvj.7349
2. Alves, R.R.N., de Araújo, B.M.C., da Silva Policarpo, I., Pereira, H.M., Borges, A.K.M., da Silva Vieira, W.L. and Vasconcellos, A. 2019. Keeping reptiles as pets in Brazil: Ethnozoological and conservation aspects. Journal for Nature Conservation, 49: 9-21. doi: 10.1016/j.jnc.2019.02.002
3. Amanatfard, E., Youssefi, M.R. and Barimani, A. 2014. Human dermatitis caused by Ophionyssus natricis, a snake mite. Iranian Journal of Parasitology, 9: 594-596.
4. Bingül, M., Doğan, S. and Doğan, S. 2017. Morphological abnormalities in some stigmaeid species of Eustigmaeus, Stigmaeus and Storchia (Acari: Raphignathoidea: Stigmaeidae). Systematic and Applied Acarology, 22: 2119-2126. doi: 10.11158/saa.22.12.7
5. Bingül, M., Doğan, S. and Doğan, S. 2018. Asymmetric variations in some species of the genus Raphignathus Dugès (Acari: Raphignathidae). Trakya University Journal of Natural Sciences, 19: 55-58. doi: 10.23902/trkjnat.334190
6. Bursali, A., Keskin, A. and Tekin, S. 2012. A review of the ticks (Acari: Ixodida) of Turkey: Species diversity, hosts and geographical distribution. Experimental and Applied Acarology, 57: 91-104. doi: 10.1007/s10493-012-9530-4
7. Dik, B. 2012. The first case of Ophionyssus natricis (Gervais, 1844) on a sea snake (Natrix tessellata, Laurente 1768) (Reptilia: Squamata: Colubridae) in Turkey. Türkiye Parazitoloji Dergisi, 36: 112-115. doi: 10.5152/tpd.2012.27
8. Evans, G.O. and Till, W.M. 1966. Studies on the British Dermanyssidae (Acari: Mesostigmata). Part II Classification. Bulletin of the British Museum (Natural History) Zoology, 14: 107-370.

9. Fisher, P. and Csurhes, S. 2009. Pest animal risk assessment American corn snake Elaphe guttata. Queensland Primary Industries and Fisheries, Brisbane, Australia, 15 pp.
10. Fitzgerald, K.T. and Vera, R. 2006. Acariasis. In: Reptile medicine and surgery. Mader, D.R. (Ed). Elsevier, Saint Louis, USA, 720-738.
11. Fonseca, É., Marques, R. and Tinôco, M.S. 2014. New records of Pantherophis guttatus (Squamata: Colubridae) in the state of Bahia, an alien species to Brazil. Salamandra, 50: 241-244.
12. Gazyağcı, S., Aktaş, M.S. and Sarı, B. 2011. The first record of the mite (Hirstiella sp.) on a green iguana from Turkey and its therapy with fipronil-a case report. Veterinarski Arhiv, 81: 793-797.
13. Głowska, E. and Skoracki, M. 2009. Anomalous chaetotaxy in the quill mites Torotrogla merulae Skoracki et al., 2000 (Acari, Prostigmata, Syringophilidae). Acta Parasitologica, 54: 364-367. doi: 10.2478/s11686-009-0046-y
14. Guglielmone, A.A., Apanaskevich, D.A., Estrada-Peña, A., Robbins, R.G., Petney, T.N. and Horak, I.G. 2014. The hard ticks of the world: (Acari: Ixodida: Ixodidae). Springer, Dordrecht, The Netherlands, 738 pp.
15. Jabbarpour, S. 2016. Ectoparasit living mites on some lizard which distributed in Turkey (Arachnida: Acarina). PhD Dissertation. Department of Biology, Graduate School of Natural and Applied Science, Ege University, İzmir, Turkey, 158 pp.
16. Kalúz, S. 2011. Two new chigger mites of the genus Lacertacarus (Acari: Prostigmata, Trombiculidae). Zootaxa, 2922: 15-26. doi: 10.11646/zootaxa.2922.1.2
17. Kepka, O. 1962. Trombiculidae (Acari) aus der Türkei. Zeitschrift für Parasitenkunde, 21: 273-289. doi: 10.1007/BF00261369
18. Kepka, O. 1966. Trombiculidae (Acari) aus der Türkei. II. Zeitschrift für Parasitenkunde, 27: 43-63. doi: 10.1007/BF00261217
19. Keskin, A., Bursali, A., Kumlutas, Y., Ilgaz, C. and Tekin, S. 2013. Parasitism of immature stages of Haemaphysalis sulcata (Acari: Ixodidae) on some reptiles in Turkey. Journal of Parasitology, 99: 752-755. doi: 10.1645/13-187.1
20. Kubiak, M. 2020. Corn Snakes. In: Handbook of exotic pet medicine. Kubiak, M. (Ed.). John Wiley and Sons Ltd, New Jersey, USA, 283-304.
21. Kurtdede, A., Haydardedeoğlu, A.E. and Kar, S. 2009. Bir Boa constrictur [sic]’da Ophionyssus natricis enfeksiyonu ve sağaltımı. Kafkas Üniversitesi Veteriner Fakültesi Dergisi, 15: 323. doi: 10.9775/kvfd.2008.98-E
22. Marshall, B.M., Strine, C. and Hughes, A.C. 2020. Thousands of reptile species threatened by under-regulated global trade. Nature Communications, 11: 4738. doi: 10.1038/s41467-020-18523-4
23. McFadden, M.S., Topham, P. and Harlow, P.S. 2017. A ticking time bomb: Is the illegal pet trade a pathway for the establishment of corn snake (Elaphe guttata) populations in Australia? Australian Zoologist, 38: 499-504. doi: 10.7882/AZ.2017.006
24. Mendoza-Roldan, J.A., Modry, D. and Otranto, D. 2020. Zoonotic parasites of reptiles: a crawling threat. Trends in Parasitology, 36: 677-687. doi: 10.1016/j.pt.2020.04.014
25. Mendoza-Roldan, J.A., Ribeiro, S.R., Castilho-Onofrio, V., Marcili, A., Simonato, B.B., Latrofa, M.S., Benelli, G., Ot-ranto, D., and Barros-Battesti, D.M. 2021. Molecular detection of vector-borne agents in ectoparasites and rep-tiles from Brazil. Ticks and Tick-borne Diseases, 12: 101585. doi: 10.1016/j.ttbdis.2020.101585
26. Miranda, R.J., Cleghorn, J.E., Bermúdez, S.E. and Perotti, M.A. 2017. Occurrence of the mite Ophionyssus natricis (Acari: Macronyssidae) on captive snakes from Panama. Acarologia, 57: 365-368. doi: 10.1051/acarologia/20164161
27. Mitchell, M.A. 2007. Parasites of reptiles. In: Flynn’s parasites of laboratory animals. Baker, D.G. (Ed). Blackwell Publishing, Iowa, USA, 177-216.
28. Moraza, M.L., Irwin, N.R., Godinho, R., Baird, S.J.E. and Bellocq, J.G. 2009. A new species of Ophionyssus Mégnin (Acari: Mesostigmata: Macronyssidae) parasitic on Lacerta schreiberi Bedriaga (Reptilia: Lacertidae) from the Iberian Peninsula, and a world key to species. Zootaxa, 2007: 58-68. doi: 10.11646/zootaxa.2007.1.3
29. Norval, G., Halliday, B., Sih, A., Sharrad, R.D. and Gardner, M.G. 2020. Occurrence of the introduced snake mite, Ophionyssus natricis (Gervais, 1844), in the wild in Australia. Acarologia, 60: 559-565. doi: 10.24349/acarologia/20204385
30. Pérez, J.M. 2009. Parasites, pests, and pets in a global world: new perspectives and challenges. Journal of Exotic Pet Medicine, 18: 248-253. doi: 10.1053/j.jepm.2009.09.003
31. Petrossian, G.A., Pires, S.F. and van Uhm, D.P. 2016. An overview of seized illegal wildlife entering the United States. Global Crime, 17: 181–201. doi: 10.1080/17440572.2016.1152548
32. Reeves, W.K., Dowling, A.P. and Dasch, G.A. 2006. Rickettsial agents from parasitic Dermanyssoidea (Acari: Mesostigmata). Experimental snd Applied Acarology, 38: 181-188. doi:10.1007/s10493-006-0007-1
33. Schultz, H. 1975. Human infestation by Ophionyssus natricis snake mite. British Journal of Dermatology, 93: 695-697. doi: 10.1111/j.1365-2133.1975.tb05120.x
34. Seniczak, S., Ayyıldız, N. and Seniczak, A. 2012. Setal losses in the dorsal hysterosoma of Plateremaeoidea (Acari: Oribatida) in the light of ontogenetic studies. Journal of Natural History, 46: 411-451. doi: 10.1080/00222933.2011.640464
35. Setiyani, A.D. and Ahmadi, M.A. 2020. An overview of illegal parrot trade in Maluku and North Maluku Provinces. Forest and Society, 4: 48-60. doi: 10.24259/fs.v4i1.7316
36. Stekolnikov, A. and Daniel, M. 2012. Chigger mites (Acari: Trombiculidae) of Turkey. Zootaxa, 3216: 1-104. doi: 10.11646/zootaxa.3216.1.1
37. Till, W.M. 1957. Mesostigmatic mites living as parasites of reptiles in the Ethiopian region (Acarina: Laelaptidae). Journal of the Entomological Society of Southern Africa, 20: 120-143.
38. Wozniak, E.J. and DeNardo, D.F. 2000. The biology, clinical significance and control of the common snake mite, Ophionyssus natricis, in captive reptiles. Journal of Herpetological Medicine and Surgery, 10: 4-10. doi: 10.5818/1529-9651-10.3.4
39. Yunker, C.E. 1956. Studies on the snake mite, Ophionyssus natricis, in Nature. Science, 124: 979-980. doi: 10.1126/science.124.3229.979