HETEROGENEITY OF THE IXODES PERSULCATUS SCHULZE (ACARI: IXODIDAE) POPULATION DETERMINES THE QUALITIES OF INFECTED TICKS AS HOSTS AND VECTORS OF PARASITES

About authors:

A. N. Alekseev, Zoological Institute, Russian Academy of Sciences, Universitetskaya emb., 1, 199034 St. Petersburg,
RUSSIA
H. V. Dubinina, Zoological Institute of the Russian Academy of Sciences, Universitetskaya Emb. 1, 199034 Saint Petersburg, Russia

Annotation:

The heterogeneity of the population of Ixodes persulcatus Schulze ticks inhabiting the relatively small St. Petersburg (Russia) suburban forested territory was studied. The studied area is known as a focus of tick-borne encephalitis and borreliosis. The persistent subdivision of the studied popula-tion into two phenetically different groups was discovered. The first subgroup includes ticks with exoskeleton anomalies whilst the second one em-braces individuals without such anomalies. This phenomenon is associated by the authors with the heavy metal ion pollution. The part of the popula-tion with anomalies was as great as 45% in the beginning of the survey (1992) and equaled 31% at the end (2000), but never was smaller than 25%.

The use of enzyme malatdehydrogenase as a marker permitted to subdivide the whole studied group of ticks into 6 genotypes. Three of them, possessing the heaviest protein (1 homozygote and 2 heterozygote), were most abundant. They were combined in one so-called Is1 genogroup. Accord-ing to our hypothesis the ticks of this genogroup were the richest energetically. All ticks were ana-lysed for the presence of the tick-borne encephalitis virus as well as different species of Borrelia and Ehrlichia. When collecting ticks their reaction to abiotic factors was determined, first of all to the temperature gradients and humidity. The locomo-tor activity of the collected specimens was estimat-ed in the laboratory. It was stated that most infected ticks with anomalies were met in the 1st genogroup, which was most abundant (more than 80% of the collected specimens). The variances of reactions of ticks to temperature gradients were discovered i.g. to a difference between the soil surface and the litter temperatures. Such variances were connected with the tick pheno- and genotypes and with the types of tick infection by pathogens: by one or another or by several pathogens in different combinations. These variant reactions determined the distinctions in infected or uninfected, normal or anomalous tick appearance from the litter within a day and during the whole season. The highest abundance of infect-ed individuals was recorded among the anomalous ticks. The high intensity of infection and the greater locomotor activity of the heavier infected speci-mens were also observed among the anomalous ticks. These qualities made them the most danger-ous part of the population irrespective to their low, comparatively to normal ticks, abundance. In the surveyed focus, where men checked ticks attached to them ( 1992-2000), the correlation between mor-bidity and Borrelia-infected anomalous females' prevalence was stated.

Our research stresses the importance of study-ing the tick-borne disease vector population heter-ogeneity in various regions of the world. It is also important to study the complexes of tick parasites and host-pathogen, pathogen 1-pathogen 2, 3 (n) interfaces.
 

Bibliography:

Alekseev A.N. 1985. [The theory of connections of feeding types and digestion of blood-sucking ar-thropods with their ability to be specific vectors of transmissive diseases agents] // Parazitologiya. T. 19. Vyp. 1. P. 3-7. [In Russian]

Alekseev A.N. 1996. Tick pathogen interactions: behav-iour of infected and uninfected ticks (Ixodidae)// Acarology IX. Vol. 1. Proc. (Eds. R. Mitchell, D.J. Horn, G.R. Needham & W.C. Welbourn). Colum-bus, Ohio. P. 113-115.

Alekseev A.N. 1999. The pathogen-vector interface: a history of paradigms // Acarina. Vol. 7. No.2. P. 111-120.

Alekseev A.N., Burenkova L.A., Chunikhin S.P. 1988. [Behavioral characteristics of Ixodes persulcatus P. Sch. (Ixodidae) infected with tick-borne en-cephalitis virus] // Med. Parazitol. (Moscow). No. 2. S. 71-75. [In Russian]

Alekseev A.N., Burenkova L.A., Podboronov V.M., Chunikhin S.P. 1995. Bactericidal qualities of ixo-did tick (Acarina: Ixodidae) salivary cement plugs and their changes under the influence of a viral tick-borne pathogen // J. Med. Entomol. Vol. 32. No. 5. P. 578-582.

Alekseev, A.N., Burenkova, L.A., Vasilyeva, I.S., Dubi-nina H.V., Chunikhin, S.P. 1996. [The functioning of mixed tick-borne infection foci in Russia] // Med. Parazitol. (Moscow). No. 4. S. 9-16. [In Russian]

Alekseev A.N., Dubinina E.V. 1993. Abnormalities in Ixodes ticks (Ixodoidea, Ixodinae) // Acarina. Vol. 1. No. 1. P. 73-85.

Alekseev A.N., Dubinina H.V. 1996. Some aspects of the mite (Oppiidae) and tick (Ixodidae) pathology as a result of anthropogenic pressure// Acarology IX. Vol. 1. Proc. (Eds. R. Mitchell, D.J. Horn, G.R. Needham & W.C. Welbourn). Columbus, Ohio. P. 117-120.

Alekseev A.N., Dubinina H.V. 1997. Monitoring of the system "mites-microorganisms" as biotic compo-nents due to variations in the anthropogenic pres-sure // Monitoring of Biological Diversity. Mos-cow. P. 195-201.

Alekseev A.N., Dubinina H.V. 2000. Abiotic parameters and diurnal and seasonal activity of Borrelia-infect-ed and uninfected Ixodes persulcatus (Acarina, Ixo-didae) //J. Med. Entomol. Vol. 37. No. 1. P. 9-15.

Alekseev A.N., Dubinina H.V., Daniel M., Zharkov S.D. 1999. Rate of tick-borne pathogen prevalence and a risk of man mix-infection in a recreation zones of St. Petersburg megapolis // Proceedings of the 3rd Intern. Conf. on Urban Pests. (Eds. Wm.H. Robinson, F. Rettich, G.W. Rambo). Prague, Czech Republic, 19-22 July 1999. P. 670.

Alekseev A.N., Dubinina H. V., Semenov A.V., Burenk-ova L. A, Anisyutkin L.N. 2000. [Geno- and pheno-types of different populations of blood-sucking ticks Ixodes persulcatus Schulze (Acarina, Ixodi-dae): the prevalence of pathogens (Borrelia and Ehrlichia)] // The role of Blood-sucking Arthro-pods in Forest Ecosystems of Russia. Materials of the Conference, 3-5 October 2000. (Eds. A.K. Yuzbekova, V.G. Fedorova). Novgorod: NGU P. S. 70-75. [In Russian]

Alekseev A.N., Jensen P.M., Dubinina H.V., Smirnova L.A., Makrouchina N.A., Zharkov S.D. 2000. Pe-culiarities of behavior of taiga (Ixodes persulcatus) and sheep (Ixodes ricinus) ticks (Acarina: Ixodi-dae) determined by different methods // Folia Par-asitol. Vol. 47. No. 2. P. 147-153.

Alekseev A.N., Podboronov V.M., Burenkova, L.A. 1995. [Probable utilization of the defensive quali-ties of the vector saliva by specific tick-borne pathogens] // Parazitologiya. T. 29. Vyp. 3. S. 154-158. [In Russian]

Alekseev A.N., Semenov A.V., Dubinina H.V. 2001. Babesia prevailing in multyinfected Ixodes persul-catus (Acarina, Ixodidae) ticks only? // Exp. Appi. Acarol. [In press]

Azad A.F., Beard C.B. 1998. Rickettsial pathogens and their arthropod vectors // Emerg. Infect. Vol. 4. P. 179-186.

Beklemishev V.N. 1948. [Interface between taxonomi-cal position of pathogens and vectors of transmis-sive diseases of animals and man] // Med. Parazitol. (Moscow). T. 17. No. 5. S. 385-400. [In Russian] Burgdorfer W., Brinton P.L. 1975. Mechanisms of tran-sovarial infection of spotted fever rickettsiae in ticks // Ann. N.Y. Acad. Sci. Vol. 266. P. 61-72.

Burgdorfer W., Hayes S.F., Mavros A.J. 1981. Nonpath-ogenic rickettsiae in Dermacentor andersoni: a limiting factors for the distribution of Rickettsia rickettsi II Rickettsiae and Rickettsial Diseases. New York: London. P. 585-594.

BurkotT.R., Schneider B.S., Pieniazek N.J., Happ C.M., Rutherford J.S., Slemenda S.B., Hoffmeister E., Maupin G.O., Zeidner N.S. 2000. Babesia microti and Borrelia bissettii transmission by Ixodes spini-palpis ticks among prairie voles, Microtus ochro-gaster, in Colorado//Parasitology. Vol. 121. Part 6. P. 595-599.

Du Y. TangS.Y., Wu X.M., ZhangQ.e. 1990. [Dissem-ination and transovarial transmission of Borrelia burgdorfei in Ixodes persulcatus (Acari: Ixodidae)] // Clin. J. Vector Biol. Cont. Vol. 1. P. 367-369. [In Chinese].

Dubinina H.V., Alekseev A.N. 1994. Skeleton changes in the oribatid mites under the influence of the heavy metal ions accumulation // Acarina. Vol. 2. No. 1-2. P. 81-93.

Dubinina H.V., Fagerholm H.-P., Alekseev A.N., Ani-syutkin L.N. 1999. The first record of the Dipe-talonema sp. nematod larvae in Ixodes persulcatus (Acarina, Ixodidae) // Problems of Nematology. Abst. Third Intern. Nematol. Symp. St. Petersburg. P. 119-120. (Proc. Zool. Inst., Vol. 280).

Estrada-Pena A., Gray J.S., Kahl O. 1996. Variability in cuticular hydrocarbons and phenotypic discrimina-tion of Ixodes ricinus population (Acarina: Ixodi-dae) from Europe // Exp. Appi. Acarol. Vol. 20. P. 457-467.

Estrada-Pena A., Daniel M., Frandsen F., Gern L., Get-tinby G., Gray J.S., Jaenson T.G.T., Jongejan F., Kahl O., Korenberg E., Mehl R„ Nuttall P. A. 1998. Ixodes ricinus strains in Europe // Zent. Bl. Bakte-riol. Bd. 287. S. 185-189.

Fish D. Des Vignes F., Schwartz I., Coughlin R.T. 1996. Epidemiology of Lyme disease and human ehrli-chiosis in the Northeastern U.S.A. // Intern. Sci. Conf. "Tick-borne Viral, Rickettsial and Bacterial Infections". 24-26 September, 1996. Listvyanka, Irkutsk. Russia. Abstr. Irkutsk. P. 65-67.

Grubhoffer L., Jindrak L. 1998. Lectins and tick-patho-gen interactions: a mini-review // Folia Parasitol. Vol. 45. No. LP. 9-13.

Healy J. A. 1979. Analysis of glycerophosphate dehydrogenase variability in the tick Ixodes ricinus (Acari: Ixodidae) // Genetica. Vol. 30. No. 1. P. 19-30.

Jensen P.M., Kaufmann U., Smirnova L. Diurnal activ-ity of Ixodes ricinus in Denmark: aspects of phys-iological age and genotypic variation // Hereditas. 1999. Vol. 130. P. 325-330.

Johns R., Ohnishi J., Broadwater A., Sonenshine D.E., de Silva A.M., Hynes W.L. 2001. Contrasts in tick innate immune responses to Borrelia burgdorferi challenge: immunotolerance in Ixodes scapularis versus immunocompetence in D.ermacentor varia-bilis (Acarina: Ixodidae) // J. Med. Entomol. Vol. 38. No. l.P. 99-107.

Kondrashova Z.N. 1975. [Materials on the tick-borne encephalitis ecology (experimental research on the Ixodes persulcatus P.Sch. ticks as the environment for its existence)] // Autoreferat Dr. Sci. thesis, Moscow. 24 s. [In Russian]

Kondrashova Z.N., Kotel'nikovaG.M. 1973. [Interrela-tionships between Salmonella typhimurium and ixodid ticks] // Zhurnal Microbiol. (Moscow). No. 10. S. 135-137. [In Russian]

Korenberg E.I. 1999. [Interaction between transmissive disease agents in ixodid ticks (Ixodidae) with a mixed infection] // Parazitologiya. T. 33. Vyp. 4. P. 273-289. [In Russian]

Levin M.L., Fish D. 2000. Acquisition of coinfection and simultaneous transmission of Borrelia burg-dorferi and Ehrlichia phagocitophila by Ixodes scapularis ticks // Infection and Immunity. Vol. 68. No. 4. P. 2183-2186.

Magnarelli L.A., Andreadis T.G., Stafford III K.C., Holland C.J. 1991. Rickettsiae and Borrelia burg-dorferi in ixodid ticks // J. Clin. Microbiol. Vol. 29. No. 12. P. 2798-2804.

Moskvitina G.G., Korenberg E.I., Spielman A., Shchy-ogolovaT.V. 1995. [On frequencies of generalized infection in unfed adult ticks of the genus Ixodes in Russian and American foci of the borreliosis] // Parazitologiya. T. 29. Vyp. 5. S. 353-360. [In Russian].

Nakao M., Miyamoto K. 1992. Negative finding in detection of transovarial transmission of Borrelia burgdorferi in Japanese ixodid ticks, Ixodes persul-catus and Ixodes ovatus II Jpn. J. Sanit. Zool. Vol. 43. No. 4. P. 343-345.

Niebylski M.L., Schrumpf M.E., Burgdorfer W., Fischer E.R., Gage K.L., Schwan T.G. 1997. Rickettsia peacockii sp. nov., a new species infecting wood ticks in western Montana // Int. J. Sys. Bacteriol. Vol. 47. P. 446-452.

Pancholi P., Kolbert C.P., Mitchell P.D. 1995. Ixodes dammini {scapularis) as a potential vector of Hu-man Granulocytic Ehrlichiosis // J. Infect. Dis. Vol. 172. P. 1007-1012.

Pavlovsky E.N. 1947. [Microorganism, vector, external environment and their interrelationships] // Zoo-logicheskiy Zhurnal. T. 26. No. 4. S. 297-312. [In Russian]

Pavlovsky E.N., Soloviev V.D. 1940. [Experimental investigation of the tick-borne encephalitis virus circulation in the tick-vector body (Ixodes persul-catus)] // Archive Biol. Sci. Т. 59. S. 111-117. [In Russian]

PetrishchevaP.A. 1972. [Biocenotical relations of blood-sucking arthropods with vertebrates determining the possible routes of disease agents circulation] // Results of Natural Focality of Diseases Theory Development and Future Goals. Moscow. S. 37-67. [In Russian]

Pomerantzev B.I., Serdyukova G.V. 1947. [Ecological survey of Ixodidae ticks — vectors of spring-sum-mer encephalitis on Far East] // Parasitol. sbornik. Leningrad: Nauka. T. 9. S. 47-67. [In Russian]

Podboronov V.M., Berdyev A. 1991. [Defence mecha-nisms of the Ixodoidea ticks and their hosts (host-parasite interface)] (Ed. A.O. Tashliev). IlymPubl., Ashgabad. 240 s. [In Russian]

Piesman J., Donahue J.G., Mather T.N., Spielman A. 1986. Transovarially acquired Lyme disease spiro-chetes (.Borrelia burgdorferi) in field-collected lar-val Ixodes dammini (Acari: Ixodidae) // J. Med. Entomol. Vol. 23. P. 219.

Piesman J., Mather T.N., Donahue J.G., Levine J., Camp-bell J.D. KarakashianS.J., Spielman A. 1986. Com-parative prevalence of Babesia microti and Borre-lia burgdorferi in four populations of Ixodes dam-mini in eastern Massachusetts // Acta Tropica. Vol.
43. P. 263-270. RijpkemaS.G.T.,MolkenboerM.J.C.H.,SchoulsL.M.,

Jongehan F., Schellekens J.K.P. 1995. Simultane-ous detection and genotyping of three genomic groups of Borrelia burgdorferi sensu lato in Dutch Ixodes ricinus ticks by characterization of the amplified intergenic spacer region between 5S and 23S rRNA genes //J. Clin. Microbiol. Vol. 33. P. 3091-3095.

Safjanova V.M., Alekseev A.N. 1977. Mixed experi-mental infection of Phlebotomus papatasi (Sc.) with different species of Leishmania И Colloques Intern, du C.N.R.S. No. 239. Ecologie des Leish-manioses. Montpellier, France. P. 153-156.

Semenov A.V., Alekseev A.N. 1999. Borrelia infection rate and other qualities of the electrophoretypes of the Ixodes persulcatus tick population // 3rd Intern. Conf. "Ticks and Tick-borne Pathogens: Into the 21st Century". High Tatra Mountains, Slovakia. 30 August - 3 September 1999. Program and Ab-stracts. (Eds. M.Kazimirova, M.Labuda). P. 56.

Semenov A.V., Alekseev A.N., Dubinina H.V. 2000. Electrophoretypes, genotypes and Borrelia agents of Ixodes persulcatus ticks // Bull. Scand. Soc. Parasitol. Vol. 10. No. 2. P. 88-89.

Telford III S.R. 1996. Perpetuation of the agent of human granulocytic ehrlichiosis in a deer tick-rodent cycle // Intern. Sci. Conf. "Tick-borne Viral, Rickettsial and Bacterial Infections". 24-26 September, 1996. Listvyanka, Irkutsk. Abstracts. Irkutsk. P. 67.

Zharkov S.D., Jensen P.M., Dubinina H.V., Alekseev A.N. Anthropogenic pressure influence on the Ixo-des tick populations // Bull. Scand. Soc. Parasitol. Vol. 10. No. 2. P. 137-138.

Zharkov S.D., Dubinina H.V., Alekseev A.N., Jensen P.M. 2000. Anthropogenic pressure and changes of Ixodes tick populations in the Baltic region of Russia and Denmark// Acarina. Vol. 8. No. 2. P. 137-141.

ZilberL.A. 1939. Spring (spring-summer) endemic tick-borne encephalitis // Archive Biol. Sci. Т. 56. Vyp. 2. S. 9-37. [In Russian]