The phenomenon of attachment and feeding of unfed ticks (Ixodoidea) on fed and feeding specimens of the same or different species: biological and epidemiological issues

封面

如何引用文章

全文:

开放存取 开放存取
受限制的访问 ##reader.subscriptionAccessGranted##
受限制的访问 订阅存取

详细

Hyperparasitism, characterized by attachment and feeding of unfed ticks on engorged or feeding specimens of the same species (tick-to-tick attachment and feeding) has been extensively documented in laboratory colonies of ticks of the Ixodoidea superfamily. Existing literature generally assumes that hyperparasitism operates similarly across tick species in both main families, Argasidae and Ixodidae. However, a closer examination of the available data reveals distinct biological mechanisms underlying this phenomenon in different groups. In argasid ticks, hyperparasitism in laboratory colonies primarily involves unfed specimens stealing blood from their fed relatives, especially under stress of starvation or overcrowding. It remains uncertain whether this behavior of argasid ticks occurs under field conditions. If it does happen naturally, it may have originated as a consequence of the nidicolous lifestyle exhibited by soft ticks. In Ixodes ticks (Ixodinae or Prostriata), hyperparasitism of males on unfed or feeding females appears to be a side-effect in the male attempts to copulate while hyperparasitism in Amblyomminae (Metastriata) ticks is likely an aberration in feeding. This difference between Argasidae and Ixodidae may stem from independent adaptation to blood-feeding within the two Ixodoidea families. Experimental evidence of pathogen transmission between aggressor and victim during hyperparasitic feeding has only been demonstrated under laboratory conditions specifically in Ornithodoros species (Argasidae). The practical importance of this route of pathogen transmission is still unclear. Although there is an assumption in the literature that hyperparasitic pathogen transmission occurs in the taiga tick Ixodes persulcatus, it is important to know that no current data is available to support this presumption.

全文:

受限制的访问

作者简介

I. Uspensky

The Hebrew University of Jerusalem

编辑信件的主要联系方式.
Email: igorusp.acarina@gmail.com
以色列, Jerusalem

参考

  1. Alekseev A.N. 1991. Ecology of tick-borne encephalitis virus: part of Ixodidae ticks males in its circulation. Ecological Parasitology 1: 51–62.
  2. Alekseev A.N., Chunikhin S.P. 1990. Exchange by the tick-borne encephalitis virus between ixodid ticks simultaneously feeding on animals with subthreshold level of viremia. Meditsinskaya Parazitologiya i Parazitarnye Bolezni 2: 48–50. [In Russian].
  3. Alekseev A.N., Dubinina H.V. 1996a. Exchange of Borrelia burgdorferi between Ixodes persulcatus (Ixodidae: Acarina) sexual partners. Journal of Medical Entomology 33: 351–354.
  4. Alekseev A.N., Dubinina H.V. 1996b. Venereal and cannibalistic ways of Borrelia burgdorferi sensu lato exchange between males and females of Ixodes persulcatus (Ixodidae, Acarina). Roczniki Akademii Medycznei w Bialymstoku 41: 103–110.
  5. Alves C.L., Araujo R.N., Gontijo N.F., Pereira M.H. 2011. Importance and physiological effects of hemolymphagy in triatomines (Hemiptera: Reduviidae). Journal of Medical Entomology 48: 372–381. https://doi.org/10.1603/ME10151
  6. Arthur D.R. 1962. Ticks and Disease. Oxford, New York, Pergamon Press, 445 pp.
  7. Balashov Yu.S. 1972. Bloodsucking Ticks (Ixodoidea)—Vectors of diseases of man and animals. Miscellaneous Publications of the Entomological Society of America 8 (5): 159–376.
  8. Balashov Yu.S. 2006. The origin and evolution of parasitism on terrestrial vertebrates in insects, mites and ticks. Parazitologiya 40 (5): 409–424. [In Russian].
  9. Barber C.A. 1895. The tick pest in the tropics. Nature 52 (1339): 197–200.
  10. Beck A.F., Holscher K.H., Butler J.F. 1986. Life cycle of Ornithodoros turicata americanus (Acari: Argasidae) in the laboratory. Journal of Medical Entomology 23: 313–319. https://doi.org/10.1093/jmedent/23.3.313
  11. Beklemishev V.N. 1948. On interrelationships between systematic position of the agent and the vector of transmissible diseases of terrestrial vertebrates and man. Meditsinskaya Parazitologiya i Parazitarnye Bolezni 17 (5): 385–400. [In Russian].
  12. Bhat V.K.M. 1969. Parasitism of males of Ornithodoros (Pavlovskyella) tholozani var. crossi (Laboulene & Megnin, 1882) Argasidae: Ixodoidea, on fed nymphs and females of the same species. Journal of the Bombay Natural History Society 66: 401–403.
  13. Boshko G.V., Sklyar V.Е. 1981. Parasitism of ixodid ticks on horse flies. Meditsinskaya Parazitologiya i Parazitarnye Bolezni 3: 80–81. [In Russian].
  14. Buczek A., Bartosik K., Buczek A.M., Buczek W., Stanko M. 2019. Conspecific hyperparasitism in the Hyalomma excavatum tick and considerations on the biological and epidemiological implications of this phenomenon. Annales of Agricultural and Environmental Medicine 26: 548–554. https://doi.org/10.26444/aaem/110128
  15. Buczek A., Bartosik K., Buczek W., Buczek A.M., Kulina D., Kulisz J., Tomasiewicz K. 2018. A unique phenomenon of oral-anal contact between ticks observed in two tick species Ixodes ricinus and Dermacentor reticulatus. Annales of Agricultural and Environmental Medicine 25 (4): 686–689. https://doi.org/10.26444/aaem/99054
  16. Chebotarevich N.D. 1950. The study of epidemic (tick-borne) recurrence and Ornithodoros ticks in the Stavropol’ Region. Meditsinskaya Parazitologiya i Parazitarnye Bolezni 19 (6): 519–521 [In Russian].
  17. Dobrynina L.I. 1956. Ability of Ixodes persulcatus to attach to insects. Meditsinskaya Parazitologiya i Parazitarnye Bolezni 25 (2): 166. [In Russian].
  18. Durden L.A., Gerlach R.F., Beckmen K.B., Greiman S.E. 2018. Hyperparasitism and non-nidicolous mating by male Ixodes angustus ticks (Acari: Ixodidae). Journal of Medical Entomology 55: 766–768. https://doi.org/10.1093/jme/tjy012
  19. Ershova A.S., Vasiliyeva I.S. 1988. Age composition of Ornithodoros papillipes Bir. nymphs (Argasidae) in intra-population groups of different abundance. Parazitologiya 22 (1): 52–57. [In Russian].
  20. Filippova N.A. 1966. Argasid Ticks (Argasidae). Fauna of the USSR, Arachnoidea, V. 4, Fasc. 3. Moscow–Leningrad, Nauka, 256 pp. [In Russian].
  21. Filippova N.A. 1997. Ixodid Ticks of Subfamily Amblyomminae. Fauna of Russia and neighbouring countries, Arachnoidea, V. 4, Fasc. 5. Saint Petersburg, Nauka, 436 pp. [In Russian].
  22. Francis E. 1938. Longevity of the tick Ornithodoros turicata and of Spirochaeta recurrentis within this tick. Public Health Report 53: 2220–2241.
  23. Garrido R., Campos-Soto R., Quiroga N., Botto-Mahan C. 2021. Bloodmeal-stealing in wild-caught Mepraia spinolai (Hemiptera: Reduviidae), a sylvatic vector of Trypanosoma cruzi. Ecological Entomology 46: 681–683. https://doi.org/10.1111/een.12999
  24. Gray J.S., Estrada-Peña A., Vial L. 2014. Ecology of nidicolous ticks. Biology of Ticks, V. 2. New York, Oxford University Press, 39–60.
  25. Helmy N., Khalil G.M., Hoogstraal H. 1983. Hyperparasitism in Ornithodoros erraticus. Journal of Parasitology 69: 229–233. https://doi.org/10.2307/3281305
  26. Hoogstraal H., Clifford C.M., Keirans J.E. 1979. The Ornithodoros (Alectorobius) capensis group (Acarina: Ixodoidea: Argasidae) of the Palearctic and Oriental Regions. O. (A.) coniceps identity, bird and mammal hosts, virus infections, and distribution in Europe, Africa, and Asia. Journal of Parasitology 65: 395–407. https://doi.org/10.2307/3280282
  27. Hooker W.A., Bishopp F.C., Wood H.P., 1912. The life history and bionomics of some North American ticks. Washington, Govern. Printing Office, 239 pp.
  28. Ioffe-Uspensky I., Uspensky I. 2017. The influence of preprandial insemination on feeding and oviposition of Ixodes persulcatus females (Acari: Ixodidae) and some thoughts concerning mating strategies in ticks of the genus Ixodes. Ticks and Tick-Borne Diseases 8: 866–871. doi: 10.1016/j.ttbdis.2017.07.003
  29. Justi S.A., Galvão C. 2017. The evolutionary origin of diversity in Chagas disease vectors. Trends in Parasitology 33 (1): 42–52. https://doi.org/10.1016/j.pt.2016.11.002
  30. Khalil G.M. 1984. Fecundity-reducing pheromone in Argas (Persicargas) arboreus (Ixodoidea: Argasidae). Parasitology 88 (3): 395–402. https://doi.org/10.1017/s0031182000054664
  31. Klyushkina E.A. 1956. A rare case of cannibalism in ticks of the family Ixodidae. Zoologicheskii Zhurnal 35 (4): 614–615. [In Russian].
  32. Labruna M.B., Ahid S.M.M., Soares H.S., Suassuna A.C.D. 2007. Hyperparasitism in Amblyomma rotundatum (Acari: Ixodidae). Journal of Parasitology 93: 1531–1532. https://doi.org/10.1645/GE-1277.1
  33. Leonovich S.A. 2022. Male aphagia in ixodid ticks of the subfamily Ixodinae. Parazitologiya 56 (4): 267–281. [In Russian]. https://doi.org/10.31857/S0031184722040019
  34. Llanos-Soto S., Muñoz-Leal S., González-Acuña D. 2019. Hyperparasitism in the seabird tick Ornithodoros amblus (Acari: Argasidae). Systematic and Applied Acarology 24: 525–528. https://doi.org/10.11158/saa.24.3.16
  35. Londoño I.M. 1976. Transmission of microfilariae and infective larvae of Dipetalonema viteae (Filarioidea) among vector ticks, Ornithodoros tartakowskyi (Argasidae), and loss of microfilariae in coxal fluid. Journal of Parasitology 62: 786–788.
  36. Mans B.J., Neitz A.W.H. 2004. Adaptation of ticks to a blood-feeding environment: Evolution from a functional perspective. Insect Biochemistry and Molecular Biology 34: 1–17. https://doi.org/10.1016/j.ibmb.2003.09.002
  37. Mans B.J., Louw A.I., Neitz A.W.H. 2002. Evolution of hematophagy in ticks: Common origin for blood coagulation and platelet aggregation inhibitors from soft ticks of the genus Ornithodoros. Molecular Biology and Evolution 19 (10): 1695–1705. https://doi.org/10.1093/oxfordjournals.molbev.a003992
  38. Moorhouse D.E. 1966. Observations on copulation in Ixodes holocyclus Neumann and the feeding of the male. Journal of Medical Entomology 3: 168–171.
  39. Moorhouse D.E., Heath A.C.G. 1975. Parasitism of female ticks by males of the genus Ixodes. Journal of Medical Entomology 12: 571–572.
  40. Nilsson A. 1975. Parasitism of female Ixodes trianguliceps by the males. Oikos 26: 295–298.
  41. Norval R.A.I. 1974. Copulation and feeding in males of Ixodes pilosus Koch, 1844 (Acarina: Ixodidae). Journal of the Entomological Society of Southern Africa 37: 129–133.
  42. Ntiamoa-Baidu Y. 1986. Parasitism of female Ixodes (Afrixodes) moreli (Acari: Ixodidae) by males. Journal of Medical Entomology 23: 484–488. https://doi.org/10.1093/jmedent/23.5.484
  43. Oliver J.H. Jr., McKeever S., Pound J.M. 1986. Parasitism of larval Ixodes ticks by chigger mites and fed female Ornithodoros ticks by Ornithodoros males. Journal of Parasitology 72: 811–812. https://doi.org/10.2307/3281492
  44. Otálora-Luna F., Pérez-Sánchez A.J., Sandoval C., Aldana E. 2015. Evolution of hematophagous habit in Triatominae (Heteroptera: Reduviidae). Revista Chilena de Historia Natural 88: 4. https://doi.org/10.1186/s40693-014-0032-0
  45. Pavlovski E.N. 1941. A new vector of tick-borne recurrence, Ornithodorus nereensis Pawl., in Turkmenia. Doklady Akademii Nauk USSR 31 (4): 407–409. [In Russian].
  46. Petrishcheva P.A. 1947. Cannibalism in Ornithodorus ticks as a possible way of transmission of tick relapsing fever spirochetes. Novosti Meditsiny 5: 24–26. [In Russian].
  47. Phillips J.S., Adeyeye O., Bruni D., 1995. Respiratory metabolism of the soft tick, Ornithodoros turicata (Dugès). Experimental and Applied Acarology 19: 103–115. https://doi.org/10.1007/BF00052550
  48. Pospelova-Shtrom М.V. 1953. Ornithodorinae Ticks and Their Epidemiological Importance. Moscow, Medgiz, 236 pp. [In Russian].
  49. Rodrigues D.S., Labruna M.B., Ferreira L.L., Leite R.C. 2023. First description of conspecific hyperparasitism in Amblyomma sculptum. Ticks and Tick-Borne Diseases 14: 102092. https://doi.org/10.1016/j.ttbdis.2022.102092
  50. Roubaud E., Colas-Belcour J. 1935. Sur un Ixodidé peu connu d’Extrême-Orient Aponomma crassipes Neumann, 1901. Annales de Parasitologie Humaine et Comparée 13 (5): 424–429. https://doi.prg/10.1051/parasite/1935135424
  51. Ryckman R.E. 1951. Recent observations on cannibalism in Triatoma (Hemiptera: Reduviidae). Journal of Parasitology 37 (5): 433–434. https://doi.org/10.2307/3273249
  52. Sandoval C.M., Joya M.I., Gutierez R., Angulo V.M. 2000. Cleptohaematophagy of the triatomine bug Belminus herreri. Medical and Veterinary Entomology 14 (1): 100–101. https://doi.org/10.1046/j.1365-2915.2000.00210.x
  53. Schmidt J.O., Dom P.L., Klotz S.A. 2019. Second-best is better than nothing: Cocroaches as a viable food source for the kissing bug Triatoma recurve (Hemiptera: Reduviidae). Journal of Medical Entomology 56 (3): 651–655. https://doi.org/10.1093/jme/tjy233
  54. Sergent A. 1930. Presentation d’une nymphe de tique parasitant une autre nymphe de la même espèce. Bulletin de la Société d’Histoire Naturelle de l’Afrique du Nord 21: 195–196.
  55. Sharif M. 1930. A note on monstrosities observed in ixodid ticks. Record of the Indian Museum, Calcutta 32 (2): 107–112.
  56. Theodor O. 1932. Über Ornithodorus coniceps Canestrini in Palästina. Zeitschrift für Parasitenkunde 5: 69–79.
  57. Uspensky I. 2008. Argasid (soft) ticks (Acari: Ixodida: Argasidae). In: Capinera J.L. (ed.), Encyclopedia of Entomology, V. 1. Dordrecht, Springer Science, 283–288.
  58. Uspensky I.V. 2023. The phenomenon of attachment and feeding of unfed ticks (Ixodoidea) on fed and feeding specimens of the same or different species: terminological issues. Parazitologiya 57 (4): 310-318. [In Russian]. doi: 10.31857/S0031184723040026
  59. Uspensky I.V., Repkina L.V. 1978. Some observations on mating and fertilization in Ixodes persulcatus. Zoologicheskii Zhurnal 57 (7): 1092–1095 [In Russian].
  60. Uzakov U.Ya. 1961. Homovampirism in ixodid ticks. Zoologicheskii Zhurnal 40 (4): 608–609 [In Russian].
  61. Vasiliyeva I.S., Ershova A.S. 1980a. The influence of group density on moulting of ticks (Argasidae, Ixodoidea) in an experiment. Meditsinskaya Parazitologiya i Parazitarnye Bolezni 49 (4): 42–48. [In Russian].
  62. Vasiliyeva I.S., Ershova A.S. 1980b. The influence of Ornithodoros papillipes population density (Argasidae) on oviposition under experimental conditions. Parazitologiya 14 (5): 392–397. [In Russian].
  63. Votava C.L., Rabalais F.C., Ashley D.C. 1974. Transmission of Dipetalonema viteae by hyperparasitism in Ornithodorus tartakovskyi. Journal of Parasitology 60: 479.
  64. Wheler E.G. 1906. British ticks. The Journal of Agricultural Science 1 (4): 400–429.
  65. Williamson B.N., Schwan T.G. 2018. Conspecific hyperparasitism: an alternative route for Borrelia hermsii transmission by the tick Ornithodoros hermsi. Ticks and Tick-Borne Diseases 9: 334–339. https://doi.org/10.1016/j.ttbdis.2017.11.00

版权所有 © Russian Academy of Sciences, 2024
##common.cookie##