Ixodiphagus hookeri wasps (Hymenoptera: Encyrtidae) in two sympatric tick species Ixodes ricinus and Haemaphysalis concinna (Ixodida: Ixodidae) in the Slovak Karst (Slovakia): ecological and biological considerations

Ixodiphagus endoparasitoid wasps are natural tick enemies that can reduce their abundance. In this study, we investigated the presence of Ixodiphagus hookeri in Haemaphysalis concinna and Ixodes ricinus ticks in the Slovak Karst (southern Slovakia) and analysed the ecological and physiological relationships in the parasitoid-host system. Unfed H. concinna and I. ricinus nymphs harvested from vegetation were fed on rabbits. The engorged specimens were kept at 25 °C and 75% RH until the emergence of the adult wasps. For the first time in Europe, we found the presence of I. hookeri in two species of ticks collected in the same locality and compared their development in these tick species. The prevalence of wasps in H. concinna and I. ricinus during their spring activity was estimated at 10.64% and 27.78%, respectively. The presence of the wasps did not affect the duration of nymph feeding. Engorged wasp-infected ticks achieved higher body mass than non-infected specimens. In both tick species, there were no differences in the length of the development period and the number and sex ratio of adult I. hookeri. The analysed indicators and characteristics of the I. hookeri wasp-tick system can be used in research on tick control.

Tripartite Interactions among Ixodiphagus hookeri, Ixodes ricinus and Deer: Differential Interference with Transmission Cycles of Tick-Borne Pathogens

For the development of sustainable control of tick-borne diseases, insight is needed in biological factors that affect tick populations. Here, the ecological interactions among Ixodiphagus hookeri, Ixodes ricinus, and two vertebrate species groups were investigated in relation to their effects on tick-borne disease risk. In 1129 questing ticks, I. hookeri DNA was detected more often in I. ricinus nymphs (4.4%) than in larvae (0.5%) and not in adults. Therefore, we determined the infestation rate of I. hookeri in nymphs from 19 forest sites, where vertebrate, tick, and tick-borne pathogen communities had been previously quantified. We found higher than expected co-occurrence rates of I. hookeri with deer-associated Anaplasma phagocytophilum, and lower than expected rates with rodent-associated Borrelia afzelii and Neoehrlichia mikurensis. The prevalence of I. hookeri in nymphs varied between 0% and 16% and was positively correlated with the encounter probability of ungulates and the densities of all life stages of I. ricinus. Lastly, we investigated the emergence of I. hookeri from artificially fed, field-collected nymphs. Adult wasps emerged from seven of the 172 fed nymphs. From these observations, we inferred that I. hookeri is parasitizing I. ricinus larvae that are feeding on deer, rather than on rodents or in the vegetation. Since I. hookeri populations depend on deer abundance, the main propagation host of I. ricinus, these wasps have no apparent effect on tick populations. The presence of I. hookeri may directly interfere with the transmission cycle of A. phagocytophilum, but not with that of B. afzelii or N. mikurensis.

Methods of protection against ticks (Acari: Ixodida)

Kleszcze (Acari: Ixodida) należą do roztoczy, pasożytujących najczęściej na gadach, ptakach i ssakach. Ze względu na znaczenie epidemiologiczne, epizootiologiczne, jak również bezpośrednią szkodliwość wśród ludzi i zwierząt, zaliczają się do jednych z najgroźniejszych pasożytów zewnętrznych. Na całym świecie stwierdzono występowanie około 850 gatunków kleszczy, w Polsce, do tej pory stwierdzono 19 gatunków stale występujących w faunie naszego kraju. Bytują one w różnych siedliskach od terenów nizinnych aż po tereny górskie, zajmując takie miejsca jak: lasy, tereny zieleni, strychy budynków w tym mieszkalnych i gospodarskich, nory, jamy zwierząt, jaskinie. Coraz częstsze występowanie kleszczy w bliskim otoczeniu człowieka i zwierząt przydomowych oraz domowych stwarza idealne warunki do przenoszenia patogenów chorób odkleszczowych. Nie ma wątpliwości, że stale poszukiwane są wszelkie sposoby ochrony osobistej i działania środowiskowe, chroniące przed atakami kleszczy oraz przed konsekwencjami jakie mogą wystąpić po żerowaniu pasożyta. References: Aboelhadid, S.M., Kamel, A.A., Arafa, W.M., Shokier, K.A. (2013). Effect of Allium sativum and Allium cepa oils on different stages of Boophilus annulatus. Parasitology Research, 112(5), 1883–1890. DOI: 10.1007/s00436-013-3344-0 Angelo, I.C., Tunholi-Alves, V.M., Tunholi, V.M., Perinotto, W.M., Gôlo, P.S., Camargo, M.G., Quinelato, S., Pinheiro, J., Bittencourt, V.R. (2015). Physiological changes in Rhipicephalus microplus (Acari: Ixodidae) experimentally infected with entomopathogenic fungi. Parasitology Research, 114(1), 219–225. DOI: 10.1007/s00436-014-4181-5 Argas reflexus Fabricius: https://zeckenrollen.de/zecken/zeckenarten-in-deutschland/ Bezuidenhout, J.D., Stutterheim, C.J. (1980). A critical evaluation of the role played by the red-billed oxpecker Buphagus erythrorhynchus in the biological control of ticks. Onderstepoort Journal of Veterinary Research, 47(2), 51–75. Birkett, M.A., Hassanali, A., Hoglund, S., Pettersson, J., Pickett, J.A. (2011). Repellent activity of catmint, Nepeta cataria, and iridoid nepetalactone isomers against Afro-tropical mosquitoes, ixodid ticks and red poultry mites. Phytochemistry, 72(1), 109-14. DOI: 10.1016/j.phytochem.2010.09.016 Castellanos, A.A., Medeiros, M.C., Hamer, G.L., Morrow, M.E., Eubanks, M.D., Teel, P.D., Hamer, S.A., Light, J.E. (2016). Decreased small mammal and on-host tick abundance in association with invasive red imported fire ants (Solenopsis invicta). Biology Letters, 12(9), 20160463. DOI: 10.1098/rsbl.2016.0463 Collatz, J., Selzer, P., Fuhrmann, A., Oehme, R.M., Mackenstedt, U., Kahl, O., Steidle, J.L.M. (2010). A hidden beneficial: biology of the tick-wasp Ixodiphagus hookeri in Germany. Journal of Applied Entomology, 135(5), 351–358. DOI: 10.1111/j.1439-0418.2010.01560.x Duffy, D.C., Downer, R., Brinkley, C. (1992). The effectiveness of Helmeted Guineafowl in the control of the deer tick, the vector of Lyme disease. The Wilson Bulletin, 104, 342–345. Ghosh, S., Sharma, A.K., Kumar, S., Tiwari, S.S., Rastogi, S., Srivastava, S., Singh, M., Kumar, R., Paul, S., Ray, D.D., Rawat, A.K. (2011). In vitro and in vivo efficacy of Acorus calamus extract against Rhipicephalus (Boophilus) microplus. Parasitology Research, 108(2), 361–370. DOI: 10.1007/s00436-010-2070-0 Gliniewicz, A., Borecka, A., Przygodzka, M., Mikulak, E. (2019). Susceptibility of Dermacentor reticulatus ticks to repelents containing different active ingrediens. Przegląd epidemiologiczny, 73(1), 117–125. DOI: 10.32394/pe.73.13 Godara, R., Parveen, S., Katoch, R., Yadav, A., Katoch, M., Khajuria, J.K., Kaur, D., Ganai, A., Verma, P.K., Khajuria, V., Singh, N.K. (2015). Acaricidal activity of ethanolic extract of Artemisia absinthium against Hyalomma anatolicum ticks. Experimental and Applied Acarology, 65(1), 141–148. DOI: 10.1007/s10493-014-9843-6 Ixodes ricinus L. female: https://www.gmx.net/magazine/wissen/natur-umwelt/zecken-nutzen-33586218 Ixodiphagus hookeri Howard: http://www.zeckenhilfe.com/en/all-about-ticks/article/what-are-the-natural-enemies-of-ticks-; Ixodiphagus hookeri attacking a fed female tick: https://alchetron.com/Ixodiphagus-hookeri Martinez-Velazquez, M., Rosario-Cruz, R., Castillo-Herrera, G., Flores-Fernandez, J.M., Alvarez, A.H., Lugo-Cervantes, E. (2011). Acaricidal effect of essential oils from Lippia graveolens (Lamiales: Verbenaceae), Rosmarinus officinalis (Lamiales: Lamiaceae), and Allium sativum (Liliales: Liliaceae) against Rhipicephalus (Boophilus) microplus (Acari: Ixodidae). Journal of Medical Entomology, 48(4), 822–827. DOI: 10.1603/me10140 Pålsson, K., Jaenson, T.G., Baeckström, P., Borg-Karlson, A.K. (2008). Tick repellent substances in the essential oil of Tanacetum vulgare. Journal of Medical Entomology, 45(1), 88–93. DOI: 10.1603/0022-2585(2008)45[88:TRSITE]2.0.CO;2 Pirali-Kheirabadi, K., Teixeira da Silva, J.A. (2010). Lavandula angustifolia essential oil as a novel and promising natural candidate for tick (Rhipicephalus (Boophilus) annulatus) control. Experimental Parasitology, 126(2), 184–186. DOI: 10.1016/j.exppara.2010.04.012 Przygodzka, M., Mikulak, E., Chmielewski, T., Gliniewicz, A. (2019). Repellents as a major element in the context of prevention of tick-borne diseases. Przegląd epidemiologiczny, 73(2), 269–280. DOI: 10.32394/pe.73.25 Samish, M., Alekseev, E. (2001). Arthropods as Predators of Ticks (Ixodoidea). Journal of Medical Entomology, 38(1), 1–11. Samish, M., Alekseev, E., Glazer, I. (2000). Biocontrol of ticks by entomopathogenic nematodes. Research update. Annals of the New York Academy of Sciences, 916, 589–594. DOI: 10.1111/j.1749-6632.2000.tb05341.x Shaw, M.T., Keesing, F., McGrail, R., Ostfeld, R.S. (2003). Factors influencing the distribution of larval blacklegged ticks on rodent hosts. American Journal of Tropical Medicine and Hygiene, 68, 447–452. DOI: https://doi.org/10.4269/ajtmh.2003.68.447 Siuda, K. (1991). Kleszcze Polski (Acari: Ixodida). Część I. Zagadnienia ogólne. Warszawa, Wrocław: Wydawnictwo Naukowe PWN. [In Polish] Tanacetum vulgare L.: http://www.nic.funet.fi/pub/sci/bio/life/plants/magnoliophyta/magnoliophytina /magnoliopsida/asteraceae/tanacetum/vulgare-2.jpg

First evidence of Ixodiphagus hookeri (Hymenoptera: Encyrtidae) parasitization in Finnish castor bean ticks (Ixodes ricinus)

Ixodiphagus hookeri (Hymenoptera: Encyrtidae) is a parasitoid wasp specialized in parasitizing the larvae and nymphs of ticks (Acari: Ixodidae). As parasitized ticks die prior to reproduction, I. hookeri is seen as a prime biological control agent candidate. Despite this, little is known of their occurrence or ecology in northern Europe. The main aim of the current study was to determine whether adult wasps or parasitized ticks can be found from a tick-infested island in southwestern Finland, using field collections and molecular methods. Following the initial discovery of an adult I. hookeri female on Seili Island, we set out to collect further specimens via sweep netting and Malaise trappings between May and October 2017. Furthermore, 1310 Ixodes ricinus (1220 nymphs, 90 adults) collected from the island during 2012–2014 were screened for I. hookeri DNA using qPCR. Whereas no further wasp specimens could be collected via sweep netting or Malaise trappings, I. hookeri DNA was consistently detected in I. ricinus nymphs (annual minimum infection rates in 2012, 2013, and 2014: 2.3, 0.4, and 0.5%, respectively), whereas all adult samples were negative. Although the annually repeated detections of parasitized ticks suggest that the wasp inhabits the island, further field and molecular surveys are needed to more comprehensively determine the status and stability of the population.